The complex mechanism of antimycobacterial action of 5-fluorouracil

Chemistry and Biology

Volumn 22, Issue 1, 2015, Pages 63-75

  Singh, Vinayak ^a   Brecik, Miroslav ^b   Mukherjee, Raju ^a   Evans, Joanna C ^a   Svetlíková, Zuzana ^b   Blaško, Jaroslav ^b   Surade, Sachin ^c   Blackburn, Jonathan ^a   Warner, Digby F ^a   Mikušová, Katarína ^b   Mizrahi, Valerie ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

^b Physics and Informatics   (Slovakia)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMETABOLITE; ARABINOGALACTAN; DNA; FLOXURIDINE PHOSPHATE; FLUOROURACIL; PEPTIDOGLYCAN; RNA; THYMIDYLATE SYNTHASE; URACIL; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; CARBON; GLYCOSYLTRANSFERASE; MESSENGER RNA; PYRR PROTEIN, BACTERIA; RECOMBINANT PROTEIN; REPRESSOR PROTEIN; URACIL PHOSPHORIBOSYLTRANSFERASE;

ARTICLE; BACTERICIDAL ACTIVITY; CATALYSIS; DRUG MECHANISM; DRUG METABOLISM; ENZYME INHIBITION; GENE MUTATION; GENOTYPE; METABOLITE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; OPERON; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; STRESS; BIOSYNTHESIS; CELL WALL; CHEMISTRY; DRUG EFFECTS; GENETICS; ISOTOPE LABELING; METABOLISM; MUTATION;

MYCOBACTERIUM TUBERCULOSIS;

ANTI-BACTERIAL AGENTS; ANTIMETABOLITES; BACTERIAL PROTEINS; CARBON RADIOISOTOPES; CELL WALL; FLUOROURACIL; ISOTOPE LABELING; MUTATION; MYCOBACTERIUM TUBERCULOSIS; OPERON; PENTOSYLTRANSFERASES; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA, MESSENGER; THYMIDYLATE SYNTHASE;

EID: 84921460797     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2014.11.006     Document Type: Article

References (62)

1. G.L. Abrahams, A. Kumar, S. Savvi, A.W. Hung, S. Wen, C. Abell, C.E. Barry 3rd, D.R. Sherman, H.I. Boshoff, and V. Mizrahi Pathway-selective sensitization of Mycobacterium tuberculosis for target-based whole-cell screening Chem. Biol. 19 2012 844 854
2. F. Arsène-Ploetze, H. Nicoloff, B. Kammerer, J. Martinussen, and F. Bringel Uracil salvage pathway in Lactobacillus plantarum: Transcription and genetic studies J. Bacteriol. 188 2006 4777 4786
3. C.E. Barry, D.C. Crick, and M.R. McNeil Targeting the formation of the cell wall core of M. tuberculosis Infect. Disord. Drug Targets 7 2007 182 202
4. T. Basta, Y. Boum, J. Briffotaux, H.F. Becker, I. Lamarre-Jouenne, J.C. Lambry, S. Skouloubris, U. Liebl, M. Graille, H. van Tilbeurgh, and H. Myllykallio Mechanistic and structural basis for inhibition of thymidylate synthase ThyX Open Biol 2 2012 120120
5. B. Bean, and A. Tomasz Inhibitory effects and metabolism of 5-fluoropyrimidine derivatives in pneumococcus J. Bacteriol. 106 1971 412 420
6. B. Bean, and A. Tomasz 5-Fluoropyrimidine-resistant mutants of pneumococcus J. Bacteriol. 113 1973 1348 1355
7. M. Belánová, P. Dianisková, P.J. Brennan, G.C. Completo, N.L. Rose, T.L. Lowary, and K. Mikusová Galactosyl transferases in mycobacterial cell wall synthesis J. Bacteriol. 190 2008 1141 1145
8. S. Bhamidi, M.S. Scherman, V. Jones, D.C. Crick, J.T. Belisle, P.J. Brennan, and M.R. McNeil Detailed structural and quantitative analysis reveals the spatial organization of the cell walls of in vivo grown Mycobacterium leprae and in vitro grown Mycobacterium tuberculosis J. Biol. Chem. 286 2011 23168 23177
9. B.R. Bochner, and B.N. Ames Complete analysis of cellular nucleotides by two-dimensional thin layer chromatography J. Biol. Chem. 257 1982 9759 9769
10. H.I. Boshoff, M.B. Reed, C.E. Barry 3rd, and V. Mizrahi DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis Cell 113 2003 183 193
11. F. Bunz Thymidylate synthase and 5-fluorouracil: a cautionary tale Cancer Biol. Ther. 7 2008 995 996
12. P. Chander, K.M. Halbig, J.K. Miller, C.J. Fields, H.K. Bonner, G.K. Grabner, R.L. Switzer, and J.L. Smith Structure of the nucleotide complex of PyrR, the pyr attenuation protein from Bacillus caldolyticus, suggests dual regulation by pyrimidine and purine nucleotides J. Bacteriol. 187 2005 1773 1782
13. S.S. Cohen, J.G. Flaks, H.D. Barner, M.R. Loeb, and J. Lichtenstein The mode of action of 5-fluorouracil and its derivatives Proc. Natl. Acad. Sci. U S A 44 1958 1004 1012
14. J. Cox, and M. Mann MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 26 2008 1367 1372
15. S.L. Davis, N.A. Be, G. Lamichhane, S. Nimmagadda, M.G. Pomper, W.R. Bishai, and S.K. Jain Bacterial thymidine kinase as a non-invasive imaging reporter for Mycobacterium tuberculosis in live animals PLoS ONE 4 2009 e6297
16. S.S. Dawes, D.F. Warner, L. Tsenova, J. Timm, J.D. McKinney, G. Kaplan, H. Rubin, and V. Mizrahi Ribonucleotide reduction in Mycobacterium tuberculosis: function and expression of genes encoding class Ib and class II ribonucleotide reductases Infect. Immun. 71 2003 6124 6131
17. S. Ehrt, X.V. Guo, C.M. Hickey, M. Ryou, M. Monteleone, L.W. Riley, and D. Schnappinger Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor Nucleic Acids Res. 33 2005 e21
18. C.J. Fields, and R.L. Switzer Regulation of pyr gene expression in Mycobacterium smegmatis by PyrR-dependent translational repression J. Bacteriol. 189 2007 6236 6245
19. A.S. Fivian-Hughes, J. Houghton, and E.O. Davis Mycobacterium tuberculosis thymidylate synthase gene thyX is essential and potentially bifunctional, while thyA deletion confers resistance to p-aminosalicylic acid Microbiology 158 2012 308 318
20. R.C. Goldman, and B.E. Laughon Discovery and validation of new antitubercular compounds as potential drug leads and probes Tuberculosis (Edinb.) 89 2009 331 333
21. S.S. Grant, T. Kawate, P.P. Nag, M.R. Silvis, K. Gordon, S.A. Stanley, E. Kazyanskaya, R. Nietupski, A. Golas, and M. Fitzgerald Identification of novel inhibitors of nonreplicating Mycobacterium tuberculosis using a carbon starvation model ACS Chem. Biol. 8 2013 2224 2234
22. M. Gustavsson, and H. Ronne Evidence that tRNA modifying enzymes are important in vivo targets for 5-fluorouracil in yeast RNA 14 2008 666 674
23. C. Heidelberger, N.K. Chaudhuri, P. Danneberg, D. Mooren, L. Griesbach, R. Duschinsky, R.J. Schnitzer, E. Pleven, and J. Scheiner Fluorinated pyrimidines, a new class of tumour-inhibitory compounds Nature 179 1957 663 666
24. B.J. Hindson, K.D. Ness, D.A. Masquelier, P. Belgrader, N.J. Heredia, A.J. Makarewicz, I.J. Bright, M.Y. Lucero, A.L. Hiddessen, and T.C. Legler High-throughput droplet digital PCR system for absolute quantitation of DNA copy number Anal. Chem. 83 2011 8604 8610
25. J.H. Hunter, R. Gujjar, C.K. Pang, and P.K. Rathod Kinetics and ligand-binding preferences of Mycobacterium tuberculosis thymidylate synthases, ThyA and ThyX PLoS ONE 3 2008 e2237
26. T.R. Ioerger, T. O'Malley, R. Liao, K.M. Guinn, M.J. Hickey, N. Mohaideen, K.C. Murphy, H.I. Boshoff, V. Mizrahi, and E.J. Rubin Identification of new drug targets and resistance mechanisms in Mycobacterium tuberculosis PLoS ONE 8 2013 e75245
27. Y. Ishizaki, C. Hayashi, K. Inoue, M. Igarashi, Y. Takahashi, V. Pujari, D.C. Crick, P.J. Brennan, and A. Nomoto Inhibition of the first step in synthesis of the mycobacterial cell wall core, catalyzed by the GlcNAc-1-phosphate transferase WecA, by the novel caprazamycin derivative CPZEN-45 J. Biol. Chem. 288 2013 30309 30319
28. M. Jackson, M.R. McNeil, and P.J. Brennan Progress in targeting cell envelope biogenesis in Mycobacterium tuberculosis Future Microbiol. 8 2013 855 875
29. H.O. Kammen, C.C. Marvel, L. Hardy, and E.E. Penhoet Purification, structure, and properties of Escherichia coli tRNA pseudouridine synthase I J. Biol. Chem. 263 1988 2255 2263
30. K.A. Kantardjieff, C. Vasquez, P. Castro, N.M. Warfel, B.S. Rho, T. Lekin, C.Y. Kim, B.W. Segelke, T.C. Terwilliger, and B. Rupp Structure of pyrR (Rv1379) from Mycobacterium tuberculosis: a persistence gene and protein drug target Acta Crystallogr. D Biol. Crystallogr. 61 2005 355 364
31. M. Kögler, B. Vanderhoydonck, S. De Jonghe, J. Rozenski, K. Van Belle, J. Herman, T. Louat, A. Parchina, C. Sibley, E. Lescrinier, and P. Herdewijn Synthesis and evaluation of 5-substituted 2′-deoxyuridine monophosphate analogues as inhibitors of flavin-dependent thymidylate synthase in Mycobacterium tuberculosis J. Med. Chem. 54 2011 4847 4862
32. G.S. Kolly, F. Boldrin, C. Sala, N. Dhar, R.C. Hartkoorn, M. Ventura, A. Serafini, J.D. McKinney, R. Manganelli, and S.T. Cole Assessing the essentiality of the decaprenyl-phospho-d-arabinofuranose pathway in Mycobacterium tuberculosis using conditional mutants Mol. Microbiol. 92 2014 194 211
33. A. Kumar, M. Zhang, L. Zhu, R.P. Liao, C. Mutai, S. Hafsat, D.R. Sherman, and M.W. Wang High-throughput screening and sensitized bacteria identify an M. tuberculosis dihydrofolate reductase inhibitor with whole cell activity PLoS ONE 7 2012 e39961
34. B. Lechartier, J. Rybniker, A. Zumla, and S.T. Cole Tuberculosis drug discovery in the post-post-genomic era EMBO Mol. Med. 6 2014 158 168
35. D.B. Longley, D.P. Harkin, and P.G. Johnston 5-fluorouracil: mechanisms of action and clinical strategies Nat. Rev. Cancer 3 2003 330 338
36. J. Martinussen, and K. Hammer Cloning and characterization of upp, a gene encoding uracil phosphoribosyltransferase from Lactococcus lactis J. Bacteriol. 176 1994 6457 6463
37. J. Martinussen, P. Glaser, P.S. Andersen, and H.H. Saxild Two genes encoding uracil phosphoribosyltransferase are present in Bacillus subtilis J. Bacteriol. 177 1995 271 274
38. K. Mikusová, M. Mikus, G.S. Besra, I. Hancock, and P.J. Brennan Biosynthesis of the linkage region of the mycobacterial cell wall J. Biol. Chem. 271 1996 7820 7828
39. J.A. Mills, K. Motichka, M. Jucker, H.P. Wu, B.C. Uhlik, R.J. Stern, M.S. Scherman, V.D. Vissa, F. Pan, and M. Kundu Inactivation of the mycobacterial rhamnosyltransferase, which is needed for the formation of the arabinogalactan-peptidoglycan linker, leads to irreversible loss of viability J. Biol. Chem. 279 2004 43540 43546
40. P. Noordhuis, U. Holwerda, C.L. Van der Wilt, C.J. Van Groeningen, K. Smid, S. Meijer, H.M. Pinedo, and G.J. Peters 5-Fluorouracil incorporation into RNA and DNA in relation to thymidylate synthase inhibition of human colorectal cancers Ann. Oncol. 15 2004 1025 1032
41. J. Nurbo, D.J. Ericsson, U. Rosenström, D. Muthas, A.M. Jansson, G. Lindeberg, T. Unge, and A. Karlén Novel pseudopeptides incorporating a benzodiazepine-based turn mimetic - targeting Mycobacterium tuberculosis ribonucleotide reductase Bioorg. Med. Chem. 21 2013 1992 2000
42. J. Ollinger, T. O'Malley, J. Ahn, J. Odingo, and T. Parish Inhibition of the sole type I signal peptidase of Mycobacterium tuberculosis is bactericidal under replicating and nonreplicating conditions J. Bacteriol. 194 2012 2614 2619
43. H.J. Rogers, and H.R. Perkins 5-Fluorouracil and mucopeptide biosynthesis by Staphylococcus aureus Biochem. J. 77 1960 448 459
44. M.H. Saier Jr., V.S. Reddy, D.G. Tamang, and A. Västermark The transporter classification database Nucleic Acids Res. 42 2014 D251 D258
45. T. Samuelsson Interactions of transfer RNA pseudouridine synthases with RNAs substituted with fluorouracil Nucleic Acids Res. 19 1991 6139 6144
46. D.V. Santi, and L.W. Hardy Catalytic mechanism and inhibition of tRNA (uracil-5-)methyltransferase: evidence for covalent catalysis Biochemistry 26 1987 8599 8606
47. C.M. Sassetti, D.H. Boyd, and E.J. Rubin Genes required for mycobacterial growth defined by high density mutagenesis Mol. Microbiol. 48 2003 77 84
48. B. Schwanhäusser, D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, and M. Selbach Global quantification of mammalian gene expression control Nature 473 2011 337 342
49. S.L. Showalter, T.N. Showalter, A. Witkiewicz, R. Havens, E.P. Kennedy, T. Hucl, S.E. Kern, C.J. Yeo, and J.R. Brody Evaluating the drug-target relationship between thymidylate synthase expression and tumor response to 5-fluorouracil. Is it time to move forward? Cancer Biol. Ther. 7 2008 986 994
50. S.A. Stanley, S.S. Grant, T. Kawate, N. Iwase, M. Shimizu, C. Wivagg, M. Silvis, E. Kazyanskaya, J. Aquadro, and A. Golas Identification of novel inhibitors of M. tuberculosis growth using whole cell based high-throughput screening ACS Chem. Biol. 7 2012 1377 1384
51. R.A. Stickgold, and F.C. Neuhaus On the initial stage in peptidoglycan synthesis. Effect of 5-fluorouracil substitution on phospho-N-acetylmuramyl-pentapeptide translocase (uridine 5′-phosphate) J. Biol. Chem. 242 1967 1331 1337
52. A. Tomasz, and E. Borek The mechanism of bacterial fragility produced by 5-fluorouracil: the accumulation of cell wall precursors Proc. Natl. Acad. Sci. US A 46 1960 324 327
53. A. Tomasz, and E. Borek The mechanism of an osmotic instability induced in E. coli K-12 by 5-fluorouracil Biochemistry 1 1962 543 552
54. M. Tsukamura In vitro susceptibility of mycobacteria, especially of Mycobacterium intracellulare, to 5-fluorouracil and pattern of development of resistance of Mycobacterium tuberculosis to the drug Microbiol. Immunol. 23 1979 427 429
55. A.D. Villela, Z.A. Sánchez-Quitian, R.G. Ducati, D.S. Santos, and L.A. Basso Pyrimidine salvage pathway in Mycobacterium tuberculosis Curr. Med. Chem. 18 2011 1286 1298
56. A.D. Villela, R.G. Ducati, L.A. Rosado, C.J. Bloch, M.V. Prates, D.C. Gonçalves, C.H. Ramos, L.A. Basso, and D.S. Santos Biochemical characterization of uracil phosphoribosyltransferase from Mycobacterium tuberculosis PLoS ONE 8 2013 e56445
57. D.F. Warner, J.C. Evans, and V. Mizrahi Nucleotide metabolism and DNA replication G.F. Hatfull, W.R. Jacobs Jr. Molecular Genetics of the Mycobacteria 2nd 2014 ASM Press Washington 635 656
58. S. Yanamoto, T. Iwamoto, G. Kawasaki, I. Yoshitomi, N. Baba, and A. Mizuno Silencing of the p53R2 gene by RNA interference inhibits growth and enhances 5-fluorouracil sensitivity of oral cancer cells Cancer Lett. 223 2005 67 76
59. M.B. Yin, and Y.M. Rustum Comparative DNA strand breakage induced by FUra and FdUrd in human ileocecal adenocarcinoma (HCT-8) cells: relevance to cell growth inhibition Cancer Commun. 3 1991 45 51
60. A. Zumla, P. Nahid, and S.T. Cole Advances in the development of new tuberculosis drugs and treatment regimens Nat. Rev. Drug Discov. 12 2013 388 404
61. A. Zumla, M. Raviglione, R. Hafner, and C.F. von Reyn Tuberculosis N. Engl. J. Med. 368 2013 745 755
62. A.I. Zumla, S.H. Gillespie, M. Hoelscher, P.P. Philips, S.T. Cole, I. Abubakar, T.D. McHugh, M. Schito, M. Maeurer, and A.J. Nunn New antituberculosis drugs, regimens, and adjunct therapies: needs, advances, and future prospects Lancet Infect. Dis. 14 2014 327 340