Inactivation of the Mycobacterium tuberculosis antigen 85 complex by covalent, allosteric inhibitors

Journal of Biological Chemistry

Volumn 289, Issue 36, 2014, Pages 25031-25040

  Favrot, Lorenza ^a   Lajiness, Daniel H ^a   Ronning, Donald R ^a  

^a UNIVERSITY OF TOLEDO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ANTIGENS; BIOCHEMISTRY; CHEMICAL MODIFICATION; CRYSTAL STRUCTURE; HYDROGEN BONDS;

ALLOSTERIC INHIBITOR; CONFORMATIONAL CHANGE; COVALENT MODIFICATIONS; CYSTEINE RESIDUES; HYDROGEN BONDED NETWORK; MYCOBACTERIAL CELLS; MYCOBACTERIUM TUBERCULOSIS; X RAY CRYSTAL STRUCTURES;

COMPLEX NETWORKS;

4 CHLOROMERCURIBENZOIC ACID; ANTIGEN 85; BACTERIAL ANTIGEN; CYSTEINE; EBSELEN; GLYCINE; IODOACETAMIDE; UNCLASSIFIED DRUG; ACYLTRANSFERASE; ANTIGEN 85C, MYCOBACTERIUM TUBERCULOSIS; ENZYME INHIBITOR; NONSTEROID ANTIINFLAMMATORY AGENT; ORGANOSELENIUM DERIVATIVE; PYRROLE DERIVATIVE;

ANTIBODY COMBINING SITE; ANTIGEN FUNCTION; ARTICLE; CATALYSIS; CHEMICAL MODIFICATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; GENE INACTIVATION; HYDROGEN BOND; MUTATION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; ALLOSTERISM; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; ENZYME ACTIVATION; ENZYME ACTIVE SITE; GENETICS; METABOLISM; PROTEIN CONFORMATION; PROTEIN SECONDARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

ACYLTRANSFERASES; ALLOSTERIC REGULATION; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIGENS, BACTERIAL; AZOLES; BIOCATALYSIS; CATALYTIC DOMAIN; CHLOROMERCURIBENZOATES; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; ENZYME ACTIVATION; ENZYME INHIBITORS; HYDROGEN BONDING; IODOACETAMIDE; MODELS, MOLECULAR; MOLECULAR STRUCTURE; MUTATION; ORGANOSELENIUM COMPOUNDS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84906971948     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.582445     Document Type: Article

References (47)

1. World Health Organization (2013) Global Tuberculosis Report 2013, World Health Organization, Geneva
2. Loewenberg, S. (2012) India reports cases of totally drug-resistant tuberculosis. Lancet 379, 205
3. Vernon, A., Burman, W., Benator, D., Khan, A., and Bozeman, L. (1999) Acquired rifamycin monoresistance in patients with HIV-related tuberculosis treated with once-weekly rifapentine and isoniazid. Tuberculosis Trials Consortium. Lancet 353, 1843-1847
4. Weiner, M., Benator, D., Burman, W., Peloquin, C. A., Khan, A., Vernon, A., Jones, B., Silva-Trigo, C., Zhao, Z., and Hodge, T. (2005) Association between acquired rifamycin resistance and the pharmacokinetics of rifabutin and isoniazid among patients with HIV and tuberculosis. Clin. Infect. Dis. 40, 1481-1491
5. Boulle, A., Van Cutsem, G., Cohen, K., Hilderbrand, K., Mathee, S., Abrahams, M., Goemaere, E., Coetzee, D., and Maartens, G. (2008) Outcomes of nevirapine- and efavirenz-based antiretroviral therapy when coadministered with rifampicin-based antitubercular therapy. JAMA 300, 530-539
6. Jarlier, V., and Nikaido, H. (1994) Mycobacterial cell wall: structure and role in natural resistance to antibiotics. FEMS Microbiol. Lett. 123, 11-18
7. Crick, D. C., Mahapatra, S., and Brennan, P. J. (2001) Biosynthesis of the arabinogalactan-peptidoglycan complex of Mycobacterium tuberculosis. Glycobiology 11, 107R-118R
8. Song, H., Sandie, R., Wang, Y., Andrade-Navarro, M. A., and Niederweis, M. (2008) Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis 88, 526-544
9. Kaur, D., Guerin, M. E., Skovierová, H., Brennan, P. J., and Jackson, M. (2009) Chapter 2: Biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv. Appl. Microbiol. 69, 23-78
10. Marrakchi, H., Lanéelle, M. A., and Daffé, M. (2014) Mycolic acids: structures, biosynthesis, and beyond. Chem. Biol. 21, 67-85
11. Jackson, M., McNeil, M. R., and Brennan, P. J. (2013) Progress in targeting cell envelope biogenesis in Mycobacterium tuberculosis. Future Microbiol. 8, 855-875
12. Favrot, L., and Ronning, D. R. (2012) Targeting the mycobacterial envelope for tuberculosis drug development. Expert Rev. Anti Infect. Ther. 10, 1023-1036
13. Banerjee, A., Dubnau, E., Quemard, A., Balasubramanian, V., Um, K. S., Wilson, T., Collins, D., de Lisle, G., and Jacobs, W. R., Jr. (1994) inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263, 227-230
14. Belanger, A. E., Besra, G. S., Ford, M. E., Mikusová, K., Belisle, J. T., Brennan, P. J., and Inamine, J. M. (1996) The embAB genes of Mycobacterium avium encode an arabinosyl transferase involved in cell wall arabinan biosynthesis that is the target for the antimycobacterial drug ethambutol. Proc. Natl. Acad. Sci. U.S.A. 93, 11919-11924
15. Tahlan, K., Wilson, R., Kastrinsky, D. B., Arora, K., Nair, V., Fischer, E., Barnes, S. W., Walker, J. R., Alland, D., Barry, C. E., 3rd, and Boshoff, H. I. (2012) SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 56, 1797-1809
16. Matsumoto, M., Hashizume, H., Tomishige, T., Kawasaki, M., Tsubouchi, H., Sasaki, H., Shimokawa, Y., and Komatsu, M. (2006) OPC-67683, a nitro-dihydro-imidazooxazole derivative with promising action against tuberculosis in vitro and in mice. PLoS Med. 3, e466
17. Stover, C. K., Warrener, P., VanDevanter, D. R., Sherman, D. R., Arain, T. M., Langhorne, M. H., Anderson, S. W., Towell, J. A., Yuan, Y., McMurray, D. N., Kreiswirth, B. N., Barry, C. E., and Baker, W. R. (2000) A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis. Nature 405, 962-966
18. Makarov, V., Manina, G., Mikusova, K., Möllmann, U., Ryabova, O., Saint-Joanis, B., Dhar, N., Pasca, M. R., Buroni, S., Lucarelli, A. P., Milano, A., De Rossi, E., Belanova, M., Bobovska, A., Dianiskova, P., Kordulakova, J., Sala, C., Fullam, E., Schneider, P., McKinney, J. D., Brodin, P., Christophe, T., Waddell, S., Butcher, P., Albrethsen, J., Rosenkrands, I., Brosch, R., Nandi, V., Bharath, S., Gaonkar, S., Shandil, R. K., Balasubramanian, V., Balganesh, T., Tyagi, S., Grosset, J., Riccardi, G., and Cole, S. T. (2009) Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 324, 801-804
19. Harth, G., Lee, B. Y., Wang, J., Clemens, D. L., and Horwitz, M. A. (1996) Novel insights into the genetics, biochemistry, and immunocytochemistry of the 30-kilodalton major extracellular protein of Mycobacterium tuberculosis. Infect. Immun. 64, 3038-3047
20. 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
21. Sanki, A. K., Boucau, J., Ronning, D. R., and Sucheck, S. J. (2009) Antigen 85C-mediated acyl-transfer between synthetic acyl donors and fragments of the arabinan. Glycoconj. J. 26, 589-596
22. 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. Mol. Microbiol. 31, 1573-1587
23. Armitige, L. Y., Jagannath, C., Wanger, A. R., and Norris, S. J. (2000) Disruption of the genes encoding antigen 85A and antigen 85B of Mycobacterium tuberculosis H37Rv: effect on growth in culture and in macrophages. Infect Immun. 68, 767-778
24. Nguyen, L., Chinnapapagari, S., and Thompson, C. J. (2005) FbpA-dependent biosynthesis of trehalose dimycolate is required for the intrinsic multidrug resistance, cell wall structure, and colonial morphology of Mycobacterium smegmatis. J. Bacteriol. 187, 6603-6611
25. Ronning, D. R., Klabunde, T., Besra, G. S., Vissa, V. D., Belisle, J. T., and Sacchettini, J. C. (2000) Crystal structure of the secreted form of antigen 85C reveals potential targets for mycobacterial drugs and vaccines. Nat. Struct. Biol. 7, 141-146
26. Ronning, D. R., Vissa, V., Besra, G. S., Belisle, J. T., and Sacchettini, J. C. (2004) Mycobacterium tuberculosis antigen 85A and 85C structures confirm binding orientation and conserved substrate specificity. J. Biol. Chem. 279, 36771-36777
27. Anderson, D. H., Harth, G., Horwitz, M. A., and Eisenberg, D. (2001) An interfacial mechanism and a class of inhibitors inferred from two crystal structures of the Mycobacterium tuberculosis 30 kDa major secretory protein (antigen 85B), a mycolyl transferase. J. Mol. Biol. 307, 671-681
28. Favrot, L., Grzegorzewicz, A. E., Lajiness, D. H., Marvin, R. K., Boucau, J., Isailovic, D., Jackson, M., and Ronning, D. R. (2013) Mechanism of inhibition of Mycobacterium tuberculosis antigen 85 by ebselen. Nat. Commun. 4, 2748
29. Boucau, J., Sanki, A. K., Voss, B. J., Sucheck, S. J., and Ronning, D. R. (2009) A coupled assay measuring Mycobacterium tuberculosis antigen 85C enzymatic activity. Anal. Biochem. 385, 120-127
30. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) Protein identification and analysis tools on the ExPASy server. in The Proteomics Protocols Handbook (Walker, J. M., ed) pp. 571-607, Humana Press Inc., Totowa, NJ
31. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 27, 307-326
32. Kissinger, C. R., Gehlhaar, D. K., and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D. Biol. Crystallogr. 55, 484-491
33. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., Mc-Coy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
34. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
35. Moriarty, N. W., Grosse-Kunstleve, R. W., and Adams, P. D. (2009) electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation. Acta Crystallogr. D Biol. Crystallogr. 65, 1074-1080
36. Guzman Barron, E. S., and Singer, T. P. (1945) Studies on biological oxidations: XIX: sulfhydryl enzymes in carbohydrate metabolism. J. Biol. Chem. 157, 221-240
37. Lu, J., Vlamis-Gardikas, A., Kandasamy, K., Zhao, R., Gustafsson, T. N., Engstrand, L., Hoffner, S., Engman, L., and Holmgren, A. (2013) Inhibition of bacterial thioredoxin reductase: an antibiotic mechanism targeting bacteria lacking glutathione. FASEB J. 27, 1394-1403
38. Ravelli, R. B., and McSweeney, S. M. (2000) The "fingerprint" that x-rays can leave on structures. Structure 8, 315-328
39. Weik, M., Ravelli, R. B., Kryger, G., McSweeney, S., Raves, M. L., Harel, M., Gros, P., Silman, I., Kroon, J., and Sussman, J. L. (2000) Specific chemical and structural damage to proteins produced by synchrotron radiation. Proc. Natl. Acad. Sci. U.S.A. 97, 623-628
40. Leiros, H. K., McSweeney, S. M., and Smala˚s, A. O. (2001) Atomic resolution structures of trypsin provide insight into structural radiation damage. Acta Crystallogr. D Biol. Crystallogr. 57, 488-497
41. Yamaguchi, T., Sano, K., Takakura, K., Saito, I., Shinohara, Y., Asano, T., and Yasuhara, H. (1998) Ebselen in acute ischemic stroke: a placebo-controlled, double-blind clinical trial. Stroke 29, 12-17
42. Parnham, M., and Sies, H. (2000) Ebselen: prospective therapy for cerebral ischaemia. Expert Opin. Investig. Drugs 9, 607-619
43. Singh, N., Halliday, A. C., Thomas, J. M., Kuznetsova, O. V., Baldwin, R., Woon, E. C., Aley, P. K., Antoniadou, I., Sharp, T., Vasudevan, S. R., and Churchill, G. C. (2013) A safe lithium mimetic for bipolar disorder. Nat. Commun. 4, 1332
44. Craik, C. S., Roczniak, S., Largman, C., and Rutter, W. J. (1987) The catalytic role of the active site aspartic acid in serine proteases. Science 237, 909-913
45. 102in serine protease catalysis. Science 237, 905-909
46. Puech, V., Guilhot, C., Perez, E., Tropis, M., Armitige, L. Y., Gicquel, B., and Daffé, M. (2002) Evidence for a partial redundancy of the fibronectin-binding proteins for the transfer of mycoloyl residues onto the cell wall arabinogalactan termini of Mycobacterium tuberculosis. Mol. Microbiol. 44, 1109-1122
47. Backus, K. M., Boshoff, H. I., Barry, C. S., Boutureira, O., Patel, M. K., D'Hooge, F., Lee, S. S., Via, L. E., Tahlan, K., Barry, C. E., 3rd, and Davis, B. G. (2011) Uptake of unnatural trehalose analogs as a reporter for Mycobacterium tuberculosis. Nat. Chem. Biol. 7, 228-235