Fragment-based approaches to TB drugs

Parasitology

Volumn 145, Issue 2, 2018, Pages 184-195

  Marchetti, Chiara ^a   Chan, Daniel S H ^a   Coyne, Anthony G ^a   Abell, Chris ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

BioA; cytochrome P450; EthR; fragment based approaches; medicinal chemistry; pantothenate synthetase; tuberculosis

Indexed keywords

7,8 DIAMINOPELARGONIC SYNTHASE; ANTIGEN; COENZYME A; CYTOCHROME P450; ETHIONAMIDE; PROTEIN TYROSINE PHOSPHATASE; SYNTHETASE; TUBERCULOSTATIC AGENT; UNCLASSIFIED DRUG; VEMURAFENIB; AMINOTRANSFERASE; BACTERIAL PROTEIN; BIOA PROTEIN, BACTERIA; ETHR PROTEIN, MYCOBACTERIUM TUBERCULOSIS; PANTOTHENATE SYNTHETASE; PEPTIDE SYNTHASE; REPRESSOR PROTEIN;

ANTIBIOTIC RESISTANCE; DRUG RESEARCH; DRUG TARGETING; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TUBERCULOSIS; ANTAGONISTS AND INHIBITORS; DRUG DEVELOPMENT; DRUG EFFECT; HUMAN; MICROBIOLOGY; PROCEDURES;

BACTERIAL PROTEINS; CYTOCHROME P-450 ENZYME SYSTEM; DRUG DISCOVERY; HUMANS; MYCOBACTERIUM TUBERCULOSIS; PEPTIDE SYNTHASES; REPRESSOR PROTEINS; TRANSAMINASES; TUBERCULOSIS;

EID: 84993226944     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182016001876     Document Type: Review

References (48)

1. Barr, A. J., Ugochukwu, E., Lee, W. H., King, O. N., Filippakopoulos, P., Alfano, I., Savitsky, P., Burgess-Brown, N. A., Müller, S. And Knapp, S. (2009). Large-scale structural analysis of the classical human protein tyrosine phosphatome. Cell 136, 352-363.
2. Belin, P., Le Du, M. H., Fielding, A., Lequin, O., Jacquet, M., Charbonnier, J. B. Lecoq, A., Thai, R., Courçon, M., Masson, C., Dugave, C., Genet, R., Pernodet, J. L. And Gondry, M. (2009). Identification and structural basis of the reaction catalyzed by CYP121, an essential cytochrome P450 in Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences of the United States of America 106 (18), 7426-7431.
3. Belisle, J. T., Vissa, V. D., Sievert, T., Takayama, K., Brennan, P. J. And Besra, G. S. (1997). Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276, 1420-1422.
4. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S., Barry, C. E., Tekaia, F., Badcock, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R., Devlin, K., Feltwell, T., Gentles, S., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Krogh, A., McLean, J., Moule, S., Murphy, L., Oliver, K., Osborne, J. et al. (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537-544.
5. Congreve, M., Chessari, G., Tisi, D. And Woodhead, A. J. (2008). Recent developments in fragment based drug discovery. Journal of Medicinal Chemistry 51, 3661-3680.
6. Dai, R., Wilson, D. J., Geders, T. W., Aldrich, C. C. And Finzel, B. C. (2014). Inhibition of Mycobacterium tuberculosis transaminase BioA by Aryl Hydrazines and Hydrazides. ChemBioChem 15, 575-586.
7. Dover, L. G., Corsino, P. E., Daniels, I. R., Cocklin, I. R., Tatituri, V., Besra, G. S. And Fütterer, K. (2004). Crystal Structure of the TetR/ CamR Family Repressor Mycobacterium tuberculosis EthR Implicated in Ethionamide Resistance. Journal of Molecular Biology 340, 1095-1105.
8. Engohang-Ndong, J., Baillat, D., Aumercier, M., Bellefontaine, F., Besra, G. S., Locht, C. And Baulard, A. R. (2004). EthR, a repressor of the TetR/CamR family implicated in ethionamide resistance in mycobacteria, octamerizes cooperatively on its operator. Molecular Microbiology 51, 175-188.
9. Flipo, M., Desroses, M., Lecat-Guillet, N., Dirié, B., Carette, X., Leroux, F., Piveteau, C., Demirkaya, F., Lens, Z., Rucktooa, P., Villeret, V., Christophe, T., Jeon, H. K., Locht, C., Brodin, P., Déprez, B., Baulard, A. R. And Willand, N. (2011). Ethionamide boosters: synthesis, biological activity, and structure-activity relationships of a series of 1, 2, 4-Oxadiazole EthR inhibitors. Journal of Medicinal Chemistry 54, 2994-3010.
10. Flipo, M., Desroses, M., Lecat-Guillet, N., Villemagne, B., Blondiaux, N., Leroux, F., Piveteau, C., Mathys, V., Flament, M. P., Siepmann, J., Villeret, V., Wohlkönig, A., Wintjens, R., Soror, S. H., Christophe, T., Jeon, H. K., Locht, C., Brodin, P., Déprez, B., Baulard, A. R. And Willand, N. (2012a). Ethionamide boosters. 2. combining bioisosteric replacement and structure-based drug design to solve pharmacokinetic issues in a series of potent 1, 2, 4-Oxadiazole EthR inhibitors. Journal of Medicinal Chemistry 55, 68-83.
11. Flipo, M., Willand, N., Lecat-Guillet, N., Hounsou, C., Desroses, M., Leroux, F., Lens, Z., Villeret, V., Wohlkönig, A., Wintjens, R., Christophe, T., Kyoung Jeon, H., Locht, C., Brodin, P., Baulard, A. R. And Déprez, B. (2012b). Discovery of novel N-phenylphenoxyacetamide derivatives as EthR inhibitors and ethionamide boosters by combining high-throughput screening and synthesis. Journal of Medicinal Chemistry 55, 6391-6402.
12. Frénois, F., Engohang-Ndong, J., Locht, C., Baulard, A. R. And Villeret, V. (2004). Structure of EthR in a ligand bound conformation reveals therapeutic perspectives against tuberculosis. Molecular Cell 16, 301-307.
13. Hotta, K., Kitahara, T. And Okami, Y. (1975). Studies on the mode of action of amiclenomycin. Journal of Antibiotics 28, 222-228.
14. Hudson, S. A., McLean, K. J., Munro, A. W. And Abell, C. (2012a). Mycobacterium tuberculosis cytochrome P450 enzymes: A cohort of novel TB drug targets. Biochemical Society Transactions 40(3), 573-579.
15. Hudson, S. A., McLean, K. J., Surade, S., Yang, Y. Q., Leys, D., Ciulli, A., Munro, A. W. And Abell, A. (2012b). Application of fragment screening and merging to the discovery of inhibitors of the Mycobacterium tuberculosis cytochrome P450 CYP121. Angewandte Chemie International Edition 51, 9311-9316.
16. Hudson, S. A., Surade, S., Coyne, A. G., McLean, K. J., Leys, D., Munro, A. W. And Abell, C. (2013). Overcoming the limitations of fragment merging: rescuing a strained merged fragment series targeting Mycobacterium tuberculosis CYP121. ChemMedChem 8, 1451-1456.
17. Hung, A. W., Silvestre, H. L., Wen, S., Ciulli, A., Blundell, T. L. And Abell, C. (2009). Application of fragment growing and fragment linking to the discovery of inhibitors of Mycobacterium tuberculosis pantothenate synthetase. Angewandte Chemie International Edition 48, 8452-8456.
18. Hung, A. W., Silvestre, H. L., Wen, S., George, G. P., Boland, J., Blundell, T. L., Ciulli, A. And Abell, C. (2016). Optimization of inhibitors of Mycobacterium tuberculosis pantothenate synthetase based on group efficiency analysis. ChemMedChem 11, 38-42.
19. Jackson, M., Raynaud, C., Lanéelle, M. A., Guilhot, C., Laurent-Winter, C., Ensergueix, D., Gicquel, B. And Daffé, M. (1999). Inactivation of the antigen 85C gene profoundly affects the mycolate content and alters the permeability of the Mycobacterium tuberculosis cell envelope. Molecular Microbiology 31, 1573-1587.
20. Kavanagh, M. E., Coyne, A. G., McLean, K. J., James, G. G., Levy, C. W., Marino, L. B., de Carvalho, L. P. S., Chan, D. S. H., Hudson, S. A., Surade, S., Leys, D., Munro, A. W. And Abell, C. (2016). Fragmentbased approaches to the development of Mycobacterium tuberculosis CYP121 inhibitors. Journal of Medicinal Chemistry 59, 3272-3302.
21. Koul, A., Arnoult, E., Lounis, N., Guillemont, J. And Andries, K. (2011). The challenge for new drug discovery for tuberculosis. Nature 469, 483-490.
22. Leys, D., Mowat, C. G., McLean, K. J., Richmond, A., Chapman, S. K., Walkinshaw, M. D. And Munro, A. W. (2003). Atomic structure of Mycobacterium tuberculosis CYP121 to 106 A reveals novel features of cytochrome P450. Journal of Biological Chemistry 278, 5141-5147.
23. Mascarello, A., Mori, M., Chiaradia-Delatorre, L. D., Menegatti, A. C., Delle Monache, F., Ferrari, F., Yunes, R. A., Nunes, R. J., Terenzi, H., Botta, B. And Botta, M. (2013). Discovery of Mycobacterium tuberculosis protein tyrosine phosphatase B (PtpB) inhibitors from natural products. PLoS ONE 8, e77081.
24. Mashalidis, E., led, P., Lang, S. And Abell, C. (2013). A three-stage biophysical screening cascade for fragment-based drug discovery. Nature Protocols 8, 2309-2324.
25. McLean, K. J., Carroll, P., Lewis, D. G., Dunford, A. J., Seward, H. E., Neeli, R., Cheesman, M. R., Marsollier, L., Douglas, P., Smith, W. E., Rosenkrands, I., Cole, S. T., Leys, D., Parish, T. And Munro, A. W. (2008). Characterization of active site structure in CYP121. A cytochrome P450 essential for viability of Mycobacterium tuberculosis H37Rv. Journal of Biological Chemistry 283, 33406-33416.
26. Murray, C. W. And Blundell, T. L. (2010). Structural biology in fragment-based drug design. Current Opinion in Structural Biology 20, 497-507.
27. Nikiforov, P. O., Surade, S., Blaszczyk, M., Delorme, V., Brodin, P., Baulard, A. R., Blundell, T. L. And Abell, C. (2016). A fragment merging approach towards the development of small molecule inhibitors of Mycobacterium tuberculosis EthR for use as ethionamide boosters. Organic and Biomolecular Chemistry 14, 2318-2326.
28. Park, S. W., Klotzsche, M., Wilson, D. J., Boshoff, H. I., Eoh, H., Manjunatha, U., Blumenthal, A., Rhee, K., Barry, C. E., III, Aldrich, C. C., Ehrt, S. And Schnappinger, D. (2011). Evaluating the sensitivity of Mycobacterium tuberculosis to biotin deprtication using regulated gene expression. PLoS Pathogens 7, e1002264, 1-0.
29. Rawls, K. A., Lang, T. P., Takeuchi, J., Imamura, S., Baguley, T. D., Grundner, C., Alber, T. And Ellman, J. A. (2009). Fragment-based discovery of selective inhibitors of the Mycobacterium tuberculosis protein tyrosine phosphatase PtpA. Bioorganic and Medicinal Chemistry Letters 19, 6851-6854.
30. Sambandamurthy, V. K., Wang, X., Chen, B., Russell, R. G., Derrick, S., Collins, F. M., Morris, S. L. And Jacobs, W. R. (2002). A pantothenate auxotroph of Mycobacterium tuberculosis is highly attenuated and protects mice against tuberculosis. Nature Medicine 8, 1171-1174.
31. Scheich, C., Puetter, V. And Schade, M. (2010). Novel small molecule inhibitors of MDR Mycobacterium tuberculosis by NMR fragment screening of antigen 85 °C. Journal of Medicinal Chemistry 53, 8362-8367.
32. Schmidt, M. F., Groves, M. R. And Rademann, J. (2011). Dynamic substrate enhancement for the identification of specific, second-sitebinding fragments targeting a set of protein tyrosine phosphatases. ChemBioChem 12, 2640-2646.
33. Scott, D. E., Coyne, A. G., Hudson, S. A. And Abell, C. (2012). Fragment based approaches in drug discovery and chemical biology. Biochemistry 51, 4990-5003.
34. Shi, C. And Aldrich, C. C. (2012). Design and synthesis of potential mechanism-based inhibitors of the aminotransferase BioA involved in biotin biosynthesis. Journal of Organic Chemistry 77, 6051-6058.
35. Silvestre, H. L., Blundell, T. L., Abell, C. And Ciulli, A. (2013). Integrated biophysical approach to fragment screening and validation for fragment-based lead discovery. Proceedings of the National Academy of Sciences of the United States of America 110, 12984-12989.
36. Singh, R., Rao, V., Shakila, H., Gupta, R., Khera, A., Dhar, N., Singh, A., Koul, A., Singh, Y., Naseema, M., Narayanan, P. R., Paramasivan, C. N., Ramanathan, V. D. And Tyagi, A. K. (2003). Disruption of mptpB impairs the ability of Mycobacterium tuberculosis to survive in guinea pigs. Molecular Microbiology 50, 751-762.
37. Soellner, M. B., Rawls, K. A., Grundner, C., Alber, T. And Ellman, J. A. (2007). Fragment-based substrate activity screening method for the identification of potent inhibitors of the Mycobacterium tuberculosis phosphatase PtpB. Journal of the American Chemical Society 129, 9613-9615.
38. Spry, C., Kirk, K. And Saliba, K. J. (2008). Coenzyme A biosynthesis: An antimicrobial drug target. FEMS Microbiology Reviews 32, 56-106.
39. Surade, S., Ty, N., Hengrung, N., Lechartier, B., Cole, S. T., Abell, C. And Blundell, T. L. (2014). A structure-guided fragment-based approach for the discovery of allosteric inhibitors targeting the lipophilic binding site of transcription factor EthR. Biochemical Journal 458, 387-394.
40. Tan, L. P., Wu, H., Yang, P. Y., Kalesh, K. A., Zhang, X., Hu, M., Srinivasan, R. And Yao, S. Q. (2009). High-throughput discovery of Mycobacterium tuberculosis protein tyrosine phosphatase B (MptpB) inhibitors using click chemistry. Organic Letters 11, 5102-5105.
41. Tonks, N. K. (2006). Protein tyrosine phosphatases: from genes, to function, to disease. Nature Reviews Molecular Cell Biology 7, 833-846.
42. Vannelli, T. A., Dykman, A. And Ortiz de Montellano, P. R. (2002). The antituberculosis drug ethionamide is activated by a flavoprotein monooxygenase. Journal of Biological Chemistry 77, 12824-12829.
43. Villemagne, B., Flipo, M., Blondiaux, N., Crauste, C., Malaquin, S., Leroux, F., Piveteau, C., Villeret, V., Brodin, P., Villoutreix, B. O., Sperandio, O., Soror, S. H., Wohlkönig, A., Wintjens, R., Deprez, B., Baulard, A. R. And Willand, N. (2014). Ligand efficiency driven design of new inhibitors of Mycobacterium tuberculosis transcriptional repressor EthR using fragment growing, merging, and linking approaches. Journal of Medicinal Chemistry 57, 4876-4888.
44. Wang, S. And Eisenberg, D. (2003). Crystal structures of a pantothenate synthetase from M. Tuberculosis and its complexes with substrates and a reaction intermediate. Protein Science 12, 1097-1108.
45. Webb, M. E., Smith, A. G. And Abell, C. (2002). Biosynthesis of pantothenate. Natural Product Reports 21, 695-721.
46. Willand, N., Dirié, B., Carette, X., Bifani, P., Singhal, A., Desroses, M., Leroux, F., Willery, E., Mathys, V., Déprez-Poulain, R., Delcroix, G., Frénois, F., Aumercier, M., Locht, C., Villeret, V., Déprez, B. And Baulard, A. R. (2009). Synthetic EthR inhibitors boost antituberculous activity of ethionamide. Nature Medicine 15, 537-544.
47. Woong Park, S., Klotzsche, M., Wilson, D. J., Boshoff, H. I., Eoh, H., Manjunatha, U., Blumenthal, A., Rhee, K., Barry, C. E., III, Aldrich, C. C., Ehrt, S. And Schnappinger, D. (2011). Evaluating the sensitivity of Mycobacterium tuberculosis to biotin deprivation using regulated gene expression. PLoS Pathogens 7, e1002264.
48. World Health Organisation (2015). Global tuberculosis report, Geneva; (http://apps. who. int/iris/bitstream/10665/191102/1/9789241565059-eng. pdf?ua=1 (accessed October 2016).