Identification of exosite-targeting inhibitors of anthrax lethal factor by high-throughput screening

Chemistry and Biology

Volumn 19, Issue 7, 2012, Pages 875-882

  Bannwarth, Ludovic ^a   Goldberg, Allison B ^a   Chen, Catherine ^a   Turk, Benjamin E ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LETHAL TOXIN; METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; TOXIN; UNCLASSIFIED DRUG;

ANTHRAX; ARTICLE; BIOLOGICAL ACTIVITY; CELL CULTURE; CELL VIABILITY; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; ENZYME INHIBITION; HIGH THROUGHPUT SCREENING; LETHAL GENE; MACROPHAGE; MOLECULAR LIBRARY;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; DOSE-RESPONSE RELATIONSHIP, DRUG; HIGH-THROUGHPUT SCREENING ASSAYS; MACROPHAGES; METALLOENDOPEPTIDASES; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEASE INHIBITORS; SMALL MOLECULE LIBRARIES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84864416870     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2012.05.013     Document Type: Article

References (53)

1. M.R. Arkin, and A. Whitty The road less traveled: modulating signal transduction enzymes by inhibiting their protein-protein interactions Curr. Opin. Chem. Biol. 13 2009 284 290
2. J.K. Atwal, Y. Chen, C. Chiu, D.L. Mortensen, W.J. Meilandt, Y. Liu, C.E. Heise, K. Hoyte, W. Luk, and Y. Lu A therapeutic antibody targeting BACE1 inhibits amyloid-β production in vivo Sci. Transl. Med. 3 2011 84ra43
3. C.T. Baldari, F. Tonello, S.R. Paccani, and C. Montecucco Anthrax toxins: a paradigm of bacterial immune suppression Trends Immunol. 27 2006 434 440
4. M. Björklund, P. Heikkilä, and E. Koivunen Peptide inhibition of catalytic and noncatalytic activities of matrix metalloproteinase-9 blocks tumor cell migration and invasion J. Biol. Chem. 279 2004 29589 29597
5. P.E. Bock, P. Panizzi, and I.M. Verhamme Exosites in the substrate specificity of blood coagulation reactions J. Thromb. Haemost. 5 Suppl 1 2007 81 94
6. J.C. Burnett, E.A. Henchal, A.L. Schmaljohn, and S. Bavari The evolving field of biodefence: therapeutic developments and diagnostics Nat. Rev. Drug Discov. 4 2005 281 297
7. A.P. Chopra, S.A. Boone, X. Liang, and N.S. Duesbery Anthrax lethal factor proteolysis and inactivation of MAPK kinase J. Biol. Chem. 278 2003 9402 9406
8. I. Dell'Aica, M. Donà, F. Tonello, A. Piris, M. Mock, C. Montecucco, and S. Garbisa Potent inhibitors of anthrax lethal factor from green tea EMBO Rep. 5 2004 418 422
9. M.S. Dennis, C. Eigenbrot, N.J. Skelton, M.H. Ultsch, L. Santell, M.A. Dwyer, M.P. O'Connell, and R.A. Lazarus Peptide exosite inhibitors of factor VIIa as anticoagulants Nature 404 2000 465 470
10. M.S. Dennis, M. Roberge, C. Quan, and R.A. Lazarus Selection and characterization of a new class of peptide exosite inhibitors of coagulation factor VIIa Biochemistry 40 2001 9513 9521
11. M. Di Nisio, S. Middeldorp, and H.R. Büller Direct thrombin inhibitors N. Engl. J. Med. 353 2005 1028 1040
12. M. Drag, and G.S. Salvesen Emerging principles in protease-based drug discovery Nat. Rev. Drug Discov. 9 2010 690 701
13. N.S. Duesbery, C.P. Webb, S.H. Leppla, V.M. Gordon, K.R. Klimpel, T.D. Copeland, N.G. Ahn, M.K. Oskarsson, K. Fukasawa, K.D. Paull, and G.F. Vande Woude Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor Science 280 1998 734 737
14. M. Forino, S. Johnson, T.Y. Wong, D.V. Rozanov, A.Y. Savinov, W. Li, R. Fattorusso, B. Becattini, A.J. Orry, and D. Jung Efficient synthetic inhibitors of anthrax lethal factor Proc. Natl. Acad. Sci. USA 102 2005 9499 9504
15. M. Fridman, V. Belakhov, L.V. Lee, F.S. Liang, C.H. Wong, and T. Baasov Dual effect of synthetic aminoglycosides: antibacterial activity against Bacillus anthracis and inhibition of anthrax lethal factor Angew. Chem. Int. Ed. Engl. 44 2005 447 452
16. J.A. Hardy, J. Lam, J.T. Nguyen, T. O'Brien, and J.A. Wells Discovery of an allosteric site in the caspases Proc. Natl. Acad. Sci. USA 101 2004 12461 12466
17. J.E. Holty, D.M. Bravata, H. Liu, R.A. Olshen, K.M. McDonald, and D.K. Owens Systematic review: a century of inhalational anthrax cases from 1900 to 2005 Ann. Intern. Med. 144 2006 270 280
18. M.G. Kornacker, Z. Lai, M. Witmer, J. Ma, J. Hendrick, V.G. Lee, D.J. Riexinger, C. Mapelli, W. Metzler, and R.A. Copeland An inhibitor binding pocket distinct from the catalytic active site on human beta-APP cleaving enzyme Biochemistry 44 2005 11567 11573
19. J.L. Lauer-Fields, J.K. Whitehead, S. Li, R.P. Hammer, K. Brew, and G.B. Fields Selective modulation of matrix metalloproteinase 9 (MMP-9) functions via exosite inhibition J. Biol. Chem. 283 2008 20087 20095
20. J.L. Lauer-Fields, D. Minond, P.S. Chase, P.E. Baillargeon, S.A. Saldanha, R. Stawikowska, P. Hodder, and G.B. Fields High throughput screening of potentially selective MMP-13 exosite inhibitors utilizing a triple-helical FRET substrate Bioorg. Med. Chem. 17 2009 990 1005
21. J.D. Lawrey Biological role of lichen substances Bryologist 89 1986 111 122
22. L.V. Lee, K.E. Bower, F.S. Liang, J. Shi, D. Wu, S.J. Sucheck, P.K. Vogt, and C.H. Wong Inhibition of the proteolytic activity of anthrax lethal factor by aminoglycosides J. Am. Chem. Soc. 126 2004 4774 4775
23. C.K. Li, S.L. Pender, K.M. Pickard, V. Chance, J.A. Holloway, A. Huett, N.S. Gonçalves, J.S. Mudgett, G. Dougan, G. Frankel, and T.T. MacDonald Impaired immunity to intestinal bacterial infection in stromelysin-1 (matrix metalloproteinase-3)-deficient mice J. Immunol. 173 2004 5171 5179
24. A.J. Matheson, and K.L. Goa Desirudin: a review of its use in the management of thrombotic disorders Drugs 60 2000 679 700
25. J.A. Maynard, C.B. Maassen, S.H. Leppla, K. Brasky, J.L. Patterson, B.L. Iverson, and G. Georgiou Protection against anthrax toxin by recombinant antibody fragments correlates with antigen affinity Nat. Biotechnol. 20 2002 597 601
26. J.H. Mikkelsen, C. Gyrup, P. Kristensen, M.T. Overgaard, C.B. Poulsen, L.S. Laursen, and C. Oxvig Inhibition of the proteolytic activity of pregnancy-associated plasma protein-A by targeting substrate exosite binding J. Biol. Chem. 283 2008 16772 16780
27. D.H. Min, W.J. Tang, and M. Mrksich Chemical screening by mass spectrometry to identify inhibitors of anthrax lethal factor Nat. Biotechnol. 22 2004 717 723
28. M. Moayeri, and S.H. Leppla Cellular and systemic effects of anthrax lethal toxin and edema toxin Mol. Aspects Med. 30 2009 439 455
29. K. Molnár, and E. Farkas Current results on biological activities of lichen secondary metabolites: a review Z. Naturforsch. C: J. Biosci. 65 2010 157 173
30. M. Mourez, R.S. Kane, J. Mogridge, S. Metallo, P. Deschatelets, B.R. Sellman, G.M. Whitesides, and R.J. Collier Designing a polyvalent inhibitor of anthrax toxin Nat. Biotechnol. 19 2001 958 961
31. N. Neamati, H. Hong, A. Mazumder, S. Wang, S. Sunder, M.C. Nicklaus, G.W. Milne, B. Proksa, and Y. Pommier Depsides and depsidones as inhibitors of HIV-1 integrase: discovery of novel inhibitors through 3D database searching J. Med. Chem. 40 1997 942 951
32. M.M. Numa, L.V. Lee, C.C. Hsu, K.E. Bower, and C.H. Wong Identification of novel anthrax lethal factor inhibitors generated by combinatorial Pictet-Spengler reaction followed by screening in situ ChemBioChem 6 2005 1002 1006
33. C.M. Overall Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites Mol. Biotechnol. 22 2002 51 86
34. R.G. Panchal, A.R. Hermone, T.L. Nguyen, T.Y. Wong, R. Schwarzenbacher, J. Schmidt, D. Lane, C. McGrath, B.E. Turk, and J. Burnett Identification of small molecule inhibitors of anthrax lethal factor Nat. Struct. Mol. Biol. 11 2004 67 72
35. A. Pini, Y. Runci, C. Falciani, B. Lelli, J. Brunetti, S. Pileri, M. Fabbrini, L. Lozzi, C. Ricci, and A. Bernini Stable peptide inhibitors prevent binding of lethal and oedema factors to protective antigen and neutralize anthrax toxin in vivo Biochem. J. 395 2006 157 163
36. P. Rai, C. Padala, V. Poon, A. Saraph, S. Basha, S. Kate, K. Tao, J. Mogridge, and R.S. Kane Statistical pattern matching facilitates the design of polyvalent inhibitors of anthrax and cholera toxins Nat. Biotechnol. 24 2006 582 586
37. R. Renckens, J.J. Roelofs, S. Florquin, A.F. de Vos, H.R. Lijnen, C. van't Veer, and T. van der Poll Matrix metalloproteinase-9 deficiency impairs host defense against abdominal sepsis J. Immunol. 176 2006 3735 3741
38. A. Russo, M. Piovano, L. Lombardo, L. Vanella, V. Cardile, and J. Garbarino Pannarin inhibits cell growth and induces cell death in human prostate carcinoma DU-145 cells Anticancer Drugs 17 2006 1163 1169
39. I.A. Schepetkin, A.I. Khlebnikov, L.N. Kirpotina, and M.T. Quinn Novel small-molecule inhibitors of anthrax lethal factor identified by high-throughput screening J. Med. Chem. 49 2006 5232 5244
40. W.L. Shoop, Y. Xiong, J. Wiltsie, A. Woods, J. Guo, J.V. Pivnichny, T. Felcetto, B.F. Michael, A. Bansal, and R.T. Cummings Anthrax lethal factor inhibition Proc. Natl. Acad. Sci. USA 102 2005 7958 7963
41. P. Silhár, K. Capková, N.T. Salzameda, J.T. Barbieri, M.S. Hixon, and K.D. Janda Botulinum neurotoxin A protease: discovery of natural product exosite inhibitors J. Am. Chem. Soc. 132 2010 2868 2869
42. R.C. Spencer Bacillus anthracis J. Clin. Pathol. 56 2003 182 187
43. Y. Sugimura, M. Hosono, F. Wada, T. Yoshimura, M. Maki, and K. Hitomi Screening for the preferred substrate sequence of transglutaminase using a phage-displayed peptide library: identification of peptide substrates for TGASE 2 and Factor XIIIA J. Biol. Chem. 281 2006 17699 17706
44. F. Tonello, M. Seveso, O. Marin, M. Mock, and C. Montecucco Screening inhibitors of anthrax lethal factor Nature 418 2002 386
45. B.E. Turk Manipulation of host signalling pathways by anthrax toxins Biochem. J. 402 2007 405 417
46. B.E. Turk Discovery and development of anthrax lethal factor metalloproteinase inhibitors Curr. Pharm. Biotechnol. 9 2008 24 33
47. B.E. Turk, T.Y. Wong, R. Schwarzenbacher, E.T. Jarrell, S.H. Leppla, R.J. Collier, R.C. Liddington, and L.C. Cantley The structural basis for substrate and inhibitor selectivity of the anthrax lethal factor Nat. Struct. Mol. Biol. 11 2004 60 66
48. G. Vitale, R. Pellizzari, C. Recchi, G. Napolitani, M. Mock, and C. Montecucco Anthrax lethal factor cleaves the N-terminus of MAPKKs and induces tyrosine/threonine phosphorylation of MAPKs in cultured macrophages Biochem. Biophys. Res. Commun. 248 1998 706 711
49. G. Vitale, L. Bernardi, G. Napolitani, M. Mock, and C. Montecucco Susceptibility of mitogen-activated protein kinase kinase family members to proteolysis by anthrax lethal factor Biochem. J. 352 2000 739 745
50. M.A. Wild, H. Xin, T. Maruyama, M.J. Nolan, P.M. Calveley, J.D. Malone, M.R. Wallace, and K.S. Bowdish Human antibodies from immunized donors are protective against anthrax toxin in vivo Nat. Biotechnol. 21 2003 1305 1306
51. C.L. Wilson, A.J. Ouellette, D.P. Satchell, T. Ayabe, Y.S. López-Boado, J.L. Stratman, S.J. Hultgren, L.M. Matrisian, and W.C. Parks Regulation of intestinal alpha-defensin activation by the metalloproteinase matrilysin in innate host defense Science 286 1999 113 117
52. J.Y. Yang, and W.Y. Yang Site-specific two-color protein labeling for FRET studies using split inteins J. Am. Chem. Soc. 131 2009 11644 11645
53. 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