Assessment of methylthioadenosine/S-adenosylhomocysteine nucleosidases of Borrelia burgdorferi as targets for novel antimicrobials using a novel high-throughput method

Journal of Antimicrobial Chemotherapy

Volumn 63, Issue 6, 2009, Pages 1163-1172

  Cornell, Kenneth A ^a   Primus, Shekerah ^b   Martinez, Jorge A ^a   Parveen, Nikhat ^b  

^a Boise State University   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Bgp; Enzyme inhibitors; Fluorometric assay; Lyme disease; Spirochete

Indexed keywords

5' METHYLTHIOADENOSINE; ADENOSYLHOMOCYSTEINASE; AMPICILLIN;

ANALYTIC METHOD; ANTIMICROBIAL THERAPY; ARTICLE; BACTERIUM DETECTION; BORRELIA BURGDORFERI; CONTROLLED STUDY; DRUG EXPOSURE; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; FLUORESCENCE ANALYSIS; FLUOROMETRY; GENE EXPRESSION; HIGH THROUGHPUT SCREENING; LYME DISEASE; NONHUMAN; PROTEIN TARGETING; STRUCTURE ACTIVITY RELATION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; DRUG EVALUATION, PRECLINICAL; FORMYCINS; HUMANS; MICROBIAL VIABILITY; N-GLYCOSYL HYDROLASES; PURINE-NUCLEOSIDE PHOSPHORYLASE;

EID: 65749104018     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkp129     Document Type: Article

References (40)

1. Wormser GP, Dattwyler RJ, Shapiro ED et al. Single-dose prophylaxis against Lyme disease. Lancet Infect Dis 2007; 7: 371-3.
2. Wormser GP, Dattwyler RJ, Shapiro ED et al. The clinical assessment, treatment, and prevention of Lyme disease, human granulocytic anaplasmosis, and babesiosis: Clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 2006; 43: 1089-134.
3. Jackson CR, Boylan JA, Frye JG et al. Evidence of a conjugal erythromycin resistance element in the Lyme disease spirochete Borrelia burgdorferi. Int J Antimicrob Agents 2007; 30: 496-504.
4. Sufrin JR, Meshnick SR, Spiess AJ et al. Methionine recycling pathways and antimalarial drug design. Antimicrob Agents Chemother 1995; 39: 2511-5.
5. Duerre JA. A hydrolytic nucleosidase acting on S-adenosylho-mocysteine and on 5′-methylthioadenosine. J Biol Chem 1962; 237: 3737-41.
6. Chen X, Schauder S, Potier N et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 2002; 415: 545-9.
7. Schauder S, Bassler BL. The languages of bacteria. Genes Dev 2001; 15: 1468-80.
8. Winzer K, Hardie KR, Williams P. Bacterial cell-to-cell communication: sorry, can't talk now - gone to lunch! Curr Opin Microbiol 2002; 5: 216-22.
9. Gianotti AJ, Tower PA, Sheley JH et al. Selective killing of Klebsiella pneumoniae by 5-trifluoromethylthioribose. Chemotherapeutic exploitation of the enzyme 5-methylthioribose kinase. J Biol Chem 1990; 265: 831-7.
10. Singh V, Lee JE, Nunez S et al. Transition state structure of 50-methylthioadenosine/S-adenosylhomocysteine nucleosidase from Escherichia coli and its similarity to transition state analogues. Biochemistry 2005; 44: 11647-59.
11. Li X, Chu S, Feher VA et al. Structure-based design, synthesis, and antimicrobial activity of indazole-derived SAH/MTA nucleosidase inhibitors. J Med Chem 2003; 46: 5663-73.
12. Schramm VL, Gutierrez JA, Cordovano G et al. Transition state analogues in quorum sensing and SAM recycling. Nucleic Acids Symp Ser (Oxf) 2008; 52: 75-6.
13. Lee JE, Settembre EC, Cornell KA et al. Structural comparison of MTA phosphorylase and MTA/AdoHcy nucleosidase explains substrate preferences and identifies regions exploitable for inhibitor design. Biochemistry 2004; 43: 5159-69.
14. Lee JE, Cornell KA, Riscoe MK et al. Structure of E. coli 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase reveals similarity to the purine nucleoside phosphorylases. Structure (Camb 2001; 9: 941-53.
15. Lee JE, Singh V, Evans GB et al. Structural rationale for the affinity of pico- and femtomolar transition state analogues of Escherichia coli 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase. J Biol Chem 2005; 280: 18274-82.
16. Pajula RL, Raina A. Methylthioadenosine, a potent inhibitor of spermine synthase from bovine brain. FEBS Lett 1979; 99: 343-5.
17. Raina A, Tuomi K, Pajula RL. Inhibition of the synthesis of polyamines and macromolecules by 5′-methylthioadenosine and 5′-alkylthiotubercidins in BHK21 cells. Biochem J 1982; 204 697-703.
18. Borchardt RT, Creveling CR, Ueland PM. Biological Methylation and Drug Design. Clifton, NJ: Humana Press, 1986.
19. von Lackum K, Babb K, Riley SP et al. Functionality of Borrelia burgdorferi LuxS: The Lyme disease spirochete produces and responds to the pheromone autoinducer-2 and lacks a complete activated-methyl cycle. Int J Med Microbiol 2006; 296 Suppl 40: 92-102.
20. Singh V, Shi W, Almo SC et al. Structure and inhibition of a quorum sensing target from Streptococcus pneumoniae. Biochemistry 2006; 45: 12929-41.
21. Babb K, von Lackum K, Wattier RL et al. Synthesis of autoinducer 2 by the Lyme disease spirochete, Borrelia burgdorferi. J Bacteriol 2005; 187: 3079-87.
22. Riley SP, Bykowski T, Babb K et al. Genetic and physiological characterization of the Borrelia burgdorferi ORF BB0374- pfs-metK-luxS operon. Microbiology 2007; 153: 2304-11.
23. Parveen N, Leong JM. Identification of a candidate glycosaminoglycan-binding adhesin of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 2000; 35: 1220-34.
24. Parveen N, Cornell KA, Bono JL et al. Bgp, a secreted GAG-binding protein of B. burgdorferi strain N40, displays nucleosidase activity and is not essential for infection of immunodeficient mice. Infect Immun 2006; 74: 3016-20.
25. Fraser CM, Casjens S, Huang WM et al. Genomic sequence of a Lyme disease spirochaete Borrelia burgdorferi. Nature 1997; 390: 580-6.
26. Roth BL, Poot M, Yue ST et al. Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl Environ Microbiol 1997; 63: 2421-31.
27. Langsrud S, Sundheim G. Flow cytometry for rapid assessment of viability after exposure to a quaternary ammonium compound. J Appl Bacteriol 1996; 81: 411-8.
28. Singh V, Shi W, Evans GB et al. Picomolar transition state analogue inhibitors of human 5′-methylthioadenosine phosphorylase and X-ray structure with MT-immucillin-A. Biochemistry 2004; 43: 9-18.
29. Singh V, Evans GB, Lenz DH et al. Femtomolar transition state analogue inhibitors of 5-pm-methylthioadenosine/S-adenosylhomocysteine nucleosidase from Escherichia coli. J Biol Chem 2005; 280: 18265-73.
30. Schwede T, Kopp J, Guex N et al. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res 2003; 31: 3381-5.
31. Arnold K, Bordoli L, Kopp J et al. The SWISS-MODEL workspace: A web-based environment for protein structure homology modelling. Bioinformatics 2006; 22: 195-201.
32. Kopp J, Schwede T. The SWISS-MODEL repository of annotated three-dimensional protein structure homology models. Nucleic Acids Res 2004; 32: D230-4.
33. Lee JE, Cornell KA, Riscoe MK et al. Expression, purification, crystallization and preliminary X-ray analysis of Escherichia coli 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase. Acta Crystallogr D Biol Crystallogr 2001; 57: 150-2.
34. Montgomery RR, Schreck K, Wang X et al. Human neutrophil calprotectin reduces the susceptibility of Borrelia burgdorferi to penicillin. Infect Immun 2006; 74: 2468-72.
35. Riscoe MK, Ferro AJ, Fitchen JH. Methionine recycling as a target for antiprotozoal drug development. Parasitol Today 1989; 5: 330-3.
36. Cornell KA, Swarts WE, Barry RD et al. Characterization of recombinant Escherichia coli 5′-methylthioadenosine/ S-adenosylhomocysteine nucleosidase: Analysis of enzymatic activity and substrate specificity. Biochem Biophys Res Commun 1996; 228: 724-32.
37. Cornell KA, Winter RW, Tower PA et al. Affinity purification of 5-methylthioribose kinase and 5-methylthioadenosine/ S-adenosylhomocysteine nucleosidase from Klebsiella pneumoniae. Biochem J 1996; 317: 285-90.
38. Lee JE, Smith GD, Horvatin C et al. Structural snapshots of MTA/ AdoHcy nucleosidase along the reaction coordinate provide insights into enzyme and nucleoside flexibility during catalysis. J Mol Biol 2005; 352: 559-74.
39. Siu KK, Lee JE, Smith GD et al. Structure of Staphylococcus aureus 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase. Acta Crystallogr Sect F Struct Biol Cryst Commun 2008; 64: 343-50.
40. Lee JE, Cornell KA, Riscoe MK et al. Structure of Escherichia coli 5′-methylthioadenosine/S-adenosylhomocysteine nucleosidase inhibitor complexes provide insight into the conformational changes required for substrate binding and catalysis. J Biol Chem 2003; 278: 8761-70.