The structure of a Burkholderia pseudomallei immunophilin-inhibitor complex reveals new approaches to antimicrobial development

Biochemical Journal

Volumn 437, Issue 3, 2011, Pages 413-422

  Norville, Isobel H ^a,b   O'Shea, Katherine ^a,b   Sarkar Tyson, Mitali ^b   Zheng, Suxin ^c   Titball, Richard W ^a   Varani, Gabriele ^c   Harmer, Nicholas J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Burkholderia pseudomallei; NMR; Peptidylprolyl isomerase; Small molecule inhibitor; X ray crystallography

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CYCLOHEXIMIDE; CYCLOHEXIMIDE N ETHYLETHANOATE; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 12; IMMUNOPHILIN; IMMUNOPHILIN INHIBITOR; MACROPHAGE INFECTIVITY POTENTIATOR LIKE PROTEIN 1; PEPTIDYLPROLYL ISOMERASE; PROTEIN INHIBITOR; TACROLIMUS; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; BURKHOLDERIA PSEUDOMALLEI; CARBON NUCLEAR MAGNETIC RESONANCE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BURKHOLDERIA PSEUDOMALLEI; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNOPHILINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; TACROLIMUS BINDING PROTEINS; VIRULENCE;

BACTERIA (MICROORGANISMS); BURKHOLDERIA PSEUDOMALLEI;

EID: 79960254326     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110345     Document Type: Article

References (50)

1. Wiersinga, W. J., van der Poll, T., White, N. J., Day, N. P. and Peacock, S. J. (2006) Melioidosis: insights into the pathogenicity of Burkholderia pseudomallei. Nat. Rev. Microbiol. 4, 272-282
2. White, N. (2003) Melioidosis. Lancet 361, 1715-1722
3. Cheng, A. C. and Currie, B. J. (2005) Melioidosis: epidemiology, pathophysiology, and management. Clin. Microbiol. Rev. 18, 383-416
4. Rotz, L. D., Khan, A. S., Lillibridge, S. R., Ostroff, S. M. and Hughes, J. M. (2002) Public health assessment of potential biological terror agents. Emerg. Infect. Dis. 8, 225-230
5. Kang, C. B., Hong, Y., Dhe-Paganon, S. and Yoon, H. S. (2008) FKBP family proteins: immunophilins with versatile biological functions. Neurosignals 16, 318-325
6. Cianciotto, N. P., Eisenstein, B. I., Mody, C. H., Toews, G. B. and Engleberg, N. C. (1989) A Legionella pneumophila gene encoding a species-specific surface protein potentiates initiation of intracellular infection. Infect. Immun. 57, 1255-1262
7. Lundemose, A. G., Kay, J. E. and Pearce, J. H. (1993) Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection. Mol. Microbiol. 7, 777-783
8. Leuzzi, R., Serino, L., Scarselli, M., Savino, S., Fontana, M. R., Monaci, E., Taddei, A., Fischer, G., Rappuoli, R. and Pizza, M. (2005) Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol. Microbiol. 58, 669-681
9. Moro, A., Ruiz-Cabello, F., Fernandez-Cano, A., Stock, R. P. and Gonzalez, A. (1995) Secretion by Trypanosoma cruzi of a peptidyl-prolyl cis-trans isomerase involved in cell infection. EMBO J. 14, 2483-2490
10. Helbig, J. H., Konig, B., Knospe, H., Bubert, B., Yu, C., Luck, C. P., Riboldi-Tunnicliffe, A., Hilgenfeld, R., Jacobs, E., Hacker, J. and Fischer, G. (2003) The PPIase active site of Legionella pneumophila Mip protein is involved in the infection of eukaryotic host cells. Biol. Chem. 384, 125-137
11. Wagner, C., Khan, A. S., Kamphausen, T., Schmausser, B., Unal, C., Lorenz, U., Fischer, G., Hacker, J. and Steinert, M. (2007) Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell. Microbiol. 9, 450-462
12. Zang, N., Tang, D. J., Wei, M. L., He, Y. Q., Chen, B., Feng, J. X., Xu, J., Gan, Y. Q., Jiang, B. L. and Tang, J. L. (2007) Requirement of a mip-like gene for virulence in the phytopathogenic bacterium Xanthomonas campestris pv. campestris. Mol. Plant Microbe Interact. 20, 21-30
13. Studier, F. W. (2005) Protein production by auto-induction in high-density shaking cultures. Protein Expression Purif. 41, 207-234
14. Leslie, A. G. W. (1992) Recent changes to the MOSFLM package for processing film and image plate data., Joint CCP4 and ESF-EAMCB Newsletter on Protein Crystallography, No. 26
15. Evans, P. R. (2005) Scaling and assessment of data quality. Acta Crystallogr. Sect. D Biol. Crystallogr. 62, 72-82
16. Stein, N. (2008) CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. J. Appl. Crystallogr. 41, 641-643
17. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
18. Emsley, P., Lohkamp, B., Scott, W. G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 66, 486-501
19. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. -W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 58, 1948-1954
20. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, III, B., Snoeyink, J., Richardson, J. S. and Richardson, D. C. (2007) MOLPROBITY: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
21. 2O samples of proteins. J. Magn. Reson. B 101, 333-337
22. Muhandiram, D. R., Xu, G. Y. and Kay, L. E. (1993) An enhanced-sensitivity pure absorption gradient 4d N-15, C-13-edited NOESY experiment. J. Biomol. NMR 3, 463-470
23. Yamazaki, T., Lee, W., Revington, M., Mattiello, D. L., Dahlquist, F. W., Arrowsmith, C. H. and Kay, L. E. (1994) An HNCA pulse scheme for the backbone assignment of N-15,C-13,H-2-labeled proteins-application to a 37-kDa Trp repressor DNA complex. J. Am. Chem. Soc. 116, 6464-6465
24. Muhandiram, D. R. and Kay, L. E. (1994) Gradient-enhanced triple-resonance 3-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. B 103, 203-216
25. Peterson, R. D., Theimer, C. A., Wu, H. H. and Feigon, J. (2004) New applications of 2D filtered/edited NOESY for assignment and structure elucidation of RNA and RNA-protein complexes. J. Biomol. NMR 28, 59-67 (Pubitemid 38220160)
26. Zwahlen, C., Legault, P., Vincent, S. J. F., Greenblatt, J., Konrat, R. and Kay, L. E. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage lambda N-peptide/boxB RNA complex. J. Am. Chem. Soc. 119, 6711-6721
27. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on Unix pipes. J. Biomol. NMR 6, 277-293
28. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, P., Ulrich, E. L., Markley, J. L., Ionides, J. and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59, 687-696
29. Güntert, P. (2003) Automated NMR protein structure calculation. Prog. Nucl. Magn. Reson. Spectrosc. 43, 105-125
30. Herrmann, T., Güntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319, 209-227
31. Fischer, G., Bang, H. and Mech, C. (1984) Detection of enzyme catalysis for cis-trans-isomerization of peptide-bonds using proline-containing peptides as substrates. Biomed. Biochim. Acta 43, 1101-1111
32. Kullertz, G., Luthe, S. and Fischer, G. (1998) Semiautomated microtiter plate assay for monitoring peptidyl-prolyl cis/trans isomerase activity in normal and pathological human sera. Clin. Chem. 44, 502-508
33. Williams, J. W. and Morrison, J. F. (1979) The kinetics of reversible tight-binding inhibition. Methods Enzymol. 63, 437-467
34. Ceymann, A., Horstmann, M., Ehses, P., Schweimer, K., Paschke, A. K., Steinert, M. and Faber, C. (2008) Solution structure of the Legionella pneumophila Mip-rapamycin complex. BMC Struct. Biol. 8, 17
35. Löw, C., Neumann, P., Tidow, H., Weininger, U., Haupt, C., Friedrich-Epler, B., Scholz, C., Stubbs, M. T. and Balbach, J. (2010) Crystal structure determination and functional characterization of the metallochaperone SlyD from Thermus thermophilus. J. Mol. Biol. 398, 375-390
36. Pereira, P. J., Vega, M. C., Gonzalez-Rey, E., Fernandez-Carazo, R., Macedo-Ribeiro, S., Gomis-Ruth, F. X., Gonzalez, A. and Coll, M. (2002) Trypanosoma cruzi macrophage infectivity potentiator has a rotamase core and a highly exposed α-helix. EMBO Rep. 3, 88-94 (Pubitemid 34144821)
37. Riboldi-Tunnicliffe, A., Konig, B., Jessen, S., Weiss, M. S., Rahfeld, J., Hacker, J., Fischer, G. and Hilgenfeld, R. (2001) Crystal structure of Mip, a prolylisomerase from Legionella pneumophila . Nat. Struct. Biol. 8, 779-783
38. Wilson, K. P., Yamashita, M. M., Sintchak, M. D., Rotstein, S. H., Murcko, M. A., Boger, J., Thomson, J. A., Fitzgibbon, M. J., Black, J. R. and Navia, M. A. (1995) Comparative X-ray structures of the major binding protein for the immunosuppressant FK506 (tacrolimus) in unliganded form and in complex with FK506 and rapamycin. Acta Crystallogr. Sect. D Biol. Crystallogr. 51, 511-521
39. Huse, M., Chen, Y. G., Massague, J. and Kuriyan, J. (1999) Crystal structure of the cytoplasmic domain of the type I TGFβ receptor in complex with FKBP12. Cell 96, 425-436
40. Chelu, M. G., Danila, C. I., Gilman, C. P. and Hamilton, S. L. (2004) Regulation of ryanodine receptors by FK506 binding proteins. Trends Cardiovasc. Med. 14, 227-234
41. Huse, M., Muir, T. W., Xu, L., Chen, Y. G., Kuriyan, J. and Massague, J. (2001) The TGFβ receptor activation process: an inhibitor- to substrate-binding switch. Mol. Cell 8, 671-682 (Pubitemid 32946943)
42. Szep, S., Park, S., Boder, E. T., Van Duyne, G. D. and Saven, J. G. (2009) Structural coupling between FKBP12 and buried water. Proteins 74, 603-611
43. Wintermeyer, E., Ludwig, B., Steinert, M., Schmidt, B., Fischer, G. and Hacker, J. (1995) Influence of site specifically altered Mip proteins on intracellular survival of Legionella pneumophila in eukaryotic cells. Infect. Immun. 63, 4576-4583
44. Christner, C., Wyrwa, R., Marsch, S., Kullertz, G., Thiericke, R., Grabley, S., Schumann, D. and Fischer, G. (1999) Synthesis and cytotoxic evaluation of cycloheximide derivatives as potential inhibitors of FKBP12 with neuroregenerative properties. J. Med. Chem. 42, 3615-3622
45. Sich, C., Improta, S., Cowley, D. J., Guenet, C., Merly, J. P., Teufel, M. and Saudek, V. (2000) Solution structure of a neurotrophic ligand bound to FKBP12 and its effects on protein dynamics. Eur. J. Biochem. 267, 5342-5355
46. Sun, F., Li, P., Ding, Y., Wang, L., Bartlam, M., Shu, C., Shen, B., Jiang, H., Li, S. and Rao, Z. (2003) Design and structure-based study of new potential FKBP12 inhibitors. Biophys. J. 85, 3194-3201 (Pubitemid 37345806)
47. Cornilescu, G., Delaglio, F. and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (Pubitemid 29143535)
48. Fulton, K. F., Jackson, S. E. and Buckle, A. M. (2003) Energetic and structural analysis of the role of tryptophan 59 in FKBP12. Biochemistry 42, 2364-2372
49. Baker, N., Sept, D., Joseph, S., Holst, M. and McCammon, J. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041
50. Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G. and Baker, N. A. (2007) PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res. 35, W522-W525