Structural basis for targeting the ribosomal protein S1 of Mycobacterium tuberculosis by pyrazinamide

Molecular Microbiology

Volumn 95, Issue 5, 2015, Pages 791-803

  Yang, Juanjuan ^a   Liu, Yindi ^a   Bi, Jing ^b   Cai, Qixu ^c   Liao, Xinli ^a   Li, Wenqian ^a   Guo, Chenyun ^a   Zhang, Qian ^c   Lin, Tianwei ^c   Zhao, Yufen ^a   Wang, Honghai ^b   Liu, Jun ^b,d   Zhang, Xuelian ^b   Lin, Donghai ^a  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c XIAMEN UNIVERSITY   (China)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; LYSINE; MESSENGER RNA; PHENYLALANINE; PYRAZINAMIDE; RIBOSOMAL PROTEIN S1; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; BACTERIAL RNA; PYRAZINOIC ACID; TMRNA; TUBERCULOSTATIC AGENT;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BINDING SITE; DRUG PROTEIN BINDING; DRUG RESISTANCE; DRUG STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA BINDING; STOICHIOMETRY; ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MUTATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

MYCOBACTERIUM TUBERCULOSIS;

ANTITUBERCULAR AGENTS; CRYSTALLOGRAPHY, X-RAY; MICROBIAL SENSITIVITY TESTS; MOLECULAR STRUCTURE; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PROTEIN STRUCTURE, TERTIARY; PYRAZINAMIDE; RIBOSOMAL PROTEINS; RNA, BACTERIAL; SEQUENCE ALIGNMENT; THERMODYNAMICS;

EID: 84924061601     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12892     Document Type: Article

References (37)

1. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., etal. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
2. Alexander, D.C., Ma, J.H., Guthrie, J.L., Blair, J., Chedore, P., and Jamieson, F.B. (2012) Gene sequencing for routine verification of pyrazinamide resistance in Mycobacterium tuberculosis: a role for pncA but not rpsA. J Clin Microbiol 50: 3726-3728.
3. Aliprandi, P., Sizun, C., Perez, J., Mareuil, F., Caputo, S., Leroy, J.L., etal. (2008) S1 ribosomal protein functions in translation initiation and ribonuclease RegB activation are mediated by similar RNA-protein interactions: an NMR and SAXS analysis. J Biol Chem 283: 13289-13301.
4. Boshoff, H.I., and Mizrahi, V. (1998) Purification, gene cloning, targeted knockout, overexpression, and biochemical characterization of the major pyrazinamidase from Mycobacterium smegmatis. J Bacteriol 180: 5809-5814.
5. Boshoff, H.I., Mizrahi, V., and Barry, C.E., 3rd (2002) Effects of pyrazinamide on fatty acid synthesis by whole mycobacterial cells and purified fatty acid synthase I. J Bacteriol 184: 2167-2172.
6. Bycroft, M., Hubbard, T.J., Proctor, M., Freund, S.M., and Murzin, A.G. (1997) The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88: 235-242.
7. Chenna, R., Sugawara, H., Koike, T., Lopez, R., Gibson, T.J., Higgins, D.G., and Thompson, J.D. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
8. Collaborative Computational Project, N. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
9. 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.
10. Deryusheva, E.I., Machulin, A.V., Selivanova, O.M., and Serdyuk, I.N. (2010) The S1 ribosomal protein family contains a unique conservative domain. Mol Biol 44: 642-647.
11. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
12. Felden, B., and Gillet, R. (2011) SmpB as the handyman of tmRNA during trans-translation. RNA Biol 8: 440-449.
13. Goddard, T.D., and Kneller, D.G. (2003) SPARKY 3. San Francisco: University of California.
14. Gouet, P., Courcelle, E., Stuart, D.I., and Metoz, F. (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
15. Guo, M., Sun, Z., and Zhang, Y. (2000) Mycobacterium smegmatis has two pyrazinamidase enzymes, PncA and pzaA. J Bacteriol 182: 3881-3884.
16. Keiler, K.C. (2008) Biology of trans-translation. Annu Rev Microbiol 62: 133-151.
17. Lu, P., Haagsma, A.C., Pham, H., Maaskant, J.J., Mol, S., Lill, H., and Bald, D. (2011) Pyrazinoic acid decreases the proton motive force, respiratory ATP synthesis activity, and cellular ATP levels. Antimicrob Agents Chemother 55: 5354-5357.
18. McDermott, W., and Tompsett, R. (1954) Activation of pyrazinamide and nicotinamide in acidic environments in vitro. Am Rev Tuberc 70: 748-754.
19. McGinness, K.E., and Sauer, R.T. (2004) Ribosomal protein S1 binds mRNA and tmRNA similarly but plays distinct roles in translation of these molecules. Proc Natl Acad Sci USA 101: 13454-13459.
20. Mitchison, D.A. (1985) The action of antituberculosis drugs in short-course chemotherapy. Tubercle 66: 219-225.
21. Murzin, A.G. (1993) OB(oligonucleotide/oligosaccharide binding)-fold: common structural and functional solution for non-homologous sequences. EMBO J 12: 861-867.
22. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326.
23. Qi, H., Shimizu, Y., and Ueda, T. (2007) Ribosomal protein S1 is not essential for the trans-translation machinery. J Mol Biol 368: 845-852.
24. Salah, P., Bisaglia, M., Aliprandi, P., Uzan, M., Sizun, C., and Bontems, F. (2009) Probing the relationship between Gram-negative and Gram-positive S1 proteins by sequence analysis. Nucleic Acids Res 37: 5578-5588.
25. Scorpio, A., and Zhang, Y. (1996) Mutations in pncA, a gene encoding pyrazinamidase/nicotinamidase, cause resistance to the antituberculous drug pyrazinamide in tubercle bacillus. Nat Med 2: 662-667.
26. Shi, W., Zhang, X., Jiang, X., Yuan, H., Lee, J.S., Barry, C.E., 3rd, etal. (2011) Pyrazinamide inhibits trans-translation in Mycobacterium tuberculosis. Science 333: 1630-1632.
27. Simons, S.O., Mulder, A., van Ingen, J., Boeree, M.J., and van Soolingen, D. (2013) Role of rpsA gene sequencing in diagnosis of pyrazinamide resistance. J Clin Microbiol 51: 382.
28. Sorensen, M.A., Fricke, J., and Pedersen, S. (1998) Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J Mol Biol 280: 561-569.
29. Sreevatsan, S., Pan, X., Zhang, Y., Kreiswirth, B.N., and Musser, J.M. (1997) Mutations associated with pyrazinamide resistance in pncA of Mycobacterium tuberculosis complex organisms. Antimicrob Agents Chemother 41: 636-640.
30. Subramanian, A.R. (1983) Structure and functions of ribosomal protein S1. Prog Nucleic Acid Res Mol Biol 28: 101-142.
31. Takada, K., Takemoto, C., Kawazoe, M., Konno, T., Hanawa-Suetsugu, K., Lee, S., etal. (2007) In vitro trans-translation of Thermus thermophilus: ribosomal protein S1 is not required for the early stage of trans-translation. RNA 13: 503-510.
32. Tan, Y., Hu, Z., Zhang, T., Cai, X., Kuang, H., Liu, Y., etal. (2014) Role of pncA and rpsA Gene Sequencing in Detection of Pyrazinamide Resistance in Mycobacterium tuberculosis Isolates from Southern China. J Clin Microbiol 52: 291-297.
33. Wallace, A.C., Laskowski, R.A., and Thornton, J.M. (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8: 127-134.
34. Wower, I.K., Zwieb, C.W., Guven, S.A., and Wower, J. (2000) Binding and cross-linking of tmRNA to ribosomal protein S1, on and off the Escherichia coli ribosome. EMBO J 19: 6612-6621.
35. Zhang, Y., Scorpio, A., Nikaido, H., and Sun, Z. (1999) Role of acid pH and deficient efflux of pyrazinoic acid in unique susceptibility of Mycobacterium tuberculosis to pyrazinamide. J Bacteriol 181: 2044-2049.
36. Zhang, Y., Wade, M.M., Scorpio, A., Zhang, H., and Sun, Z. (2003) Mode of action of pyrazinamide: disruption of Mycobacterium tuberculosis membrane transport and energetics by pyrazinoic acid. J Antimicrob Chemother 52: 790-795.
37. Zimhony, O., Cox, J.S., Welch, J.T., Vilcheze, C., and Jacobs, W.R., Jr (2000) Pyrazinamide inhibits the eukaryotic-like fatty acid synthetase I (FASI) of Mycobacterium tuberculosis. Nat Med 6: 1043-1047.