Potent antimicrobial small molecules screened as inhibitors of tyrosine recombinases and Holliday junction-resolving enzymes

Molecular Diversity

Volumn 15, Issue 4, 2011, Pages 989-1005

  Rideout, Marc C ^a   Boldt, Jeffrey L ^a,b   Vahi Ferguson, Gabriel ^a   Salamon, Peter ^b   Nefzi, Adel ^a,c   Ostresh, John M ^c   Giulianotti, Marc ^c   Pinilla, Clemencia ^c   Segall, Anca M ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b GENOMATICA INC   (United States)

^c TORREY PINES INSTITUTE FOR MOLECULAR STUDIES   (United States)

Author keywords

Integrase; Combinatorial libraries; DNA repair; Holliday junction; Site specific recombination

Indexed keywords

ANTIINFECTIVE AGENT; CROSSOVER JUNCTION ENDODEOXYRIBONUCLEASE; ERYTHROMYCIN; HETEROCYCLIC COMPOUND; N METHYL AMINOCYCLIC THIOUREA; PROTEIN TYROSINE KINASE INHIBITOR; PYRROLIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BINDING AFFINITY; CONTROLLED STUDY; CYTOTOXICITY; DNA REPAIR; DRUG PURIFICATION; DRUG SYNTHESIS; ENZYME INHIBITION; ESCHERICHIA COLI; IC 50; IN VITRO STUDY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA;

2-AMINOPURINE; AMINO ACID SEQUENCE; ANIMALS; ANTI-INFECTIVE AGENTS; BACTERIA; BACTERIOPHAGE LAMBDA; DNA HELICASES; DRUG EVALUATION, PRECLINICAL; ENZYME INHIBITORS; GUANIDINE; HOLLIDAY JUNCTION RESOLVASES; MICROBIAL SENSITIVITY TESTS; PYRROLIDINES; RECOMBINATION, GENETIC; TYROSINE;

EID: 84855223328     PISSN: 13811991     EISSN: 1573501X     Source Type: Journal    
DOI: 10.1007/s11030-011-9333-2     Document Type: Article

References (42)

1. Azaro M, Landy A (2002) γ Integrase and the γ Int family. In: Craig NL et al (ed) Mobile DNA II. ASM Press, Washington, DC, pp 118-149
2. Cassell G, Klemm M, Pinilla C, Segall A (2000) Dissection of bacteriophage lambda site-specific recombination using synthetic peptide combinatorial libraries. J Mol Biol 299:1193-1202. doi:10. 1006/jmbi.2000.3828
3. KlemmM, Cheng C, Cassell G, Shuman S, SegallAM (2000) Peptide inhibitors of DNA cleavage by tyrosine recombinases and topoisomerases. J Mol Biol 299:1203-1216. doi:10.1006/jmbi.2000.3829
4. Boldt JL, Pinilla C, Segall AM (2004) Reversible inhibitors of lambda integrase-mediated recombination efficiently trap Holliday junction intermediates and form the basis of a novel assay for junction resolution. J Biol Chem 279:3472-3483. doi:10.1074/jbc.M309361200 (Pubitemid 38140586)
5. Cassell GD, Segall AM (2003) Mechanism of inhibition of sitespecific recombination by the Holliday junction-trapping pep- tide WKHYNY: insights into phage lambda integrase-mediated strand exchange. J Mol Biol 327:413-429. doi:10.1016/S0022-2836(03)00058-5 (Pubitemid 36298711)
6. Kepple KV, Patel N, Salamon P, Segall AM (2008) Interactions between branched DNAs and peptide inhibitors of DNA repair. Nucl Acids Res 36:5319-5334. doi:10.1093/nar/gkn512
7. Gunderson CW, Boldt JL, Authement RN, Segall AM (2009) Peptide wrwycr inhibits the excision of several prophages and traps Holliday junctions inside bacteria. J Bacteriol 191:2169-2176. doi:10.1128/JB.01559-08
8. Gunderson CW, Segall AM (2006) DNA repair, a novel antibacterial target: Holliday junction-trapping peptides induce DNA damage and chromosome segregation defects. Mol Microbiol 59:1129-1148. doi:10.1111/j.1365-2958.2005.05009.x
9. Kepple KV, Boldt JL, Segall AM (2005) Holliday junctionbinding peptides inhibit distinct junction-processing enzymes. Proc Natl Acad Sci USA 102:6867-6872. doi:10.1073/pnas. 0409496102 (Pubitemid 40675408)
10. Segall AM, Nash HA (1996) Architectural flexibility in lambda site-specific recombination: three alternate conformations channel the attL site into three distinct pathways. Genes Cells 1:453-463. doi:10.1046/j.1365-2443. 1996.d01-254.x (Pubitemid 126673141)
11. Grindley ND, Whiteson KL, Rice PA (2006) Mechanisms of sitespecific recombination. Annu Rev Biochem 75:567-605. doi:10.1146/annurev.biochem.73. 011303.073908 (Pubitemid 44118044)
12. Fujimoto DF, Pinilla C, Segall AM (2006) New peptide inhibitors of type IB topoisomerases: similarities and differences vis-avis inhibitors of tyrosine recombinases. J Mol Biol 363:891-907. doi:10.1016/j.jmb.2006.08.052 (Pubitemid 44573227)
13. Cheng C, Kussie P, Pavletich N, Shuman S (1998) Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92:841-850. doi:S0092-8674(00)81411-7 (Pubitemid 28155322)
14. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369-413. doi:10.1146/annurev.biochem.70.1.369 (Pubitemid 32662215)
15. Lilley DM (2008) Analysis of branched nucleic acid structure using comparative gel electrophoresis. Q Rev Biophys 41:1-39. doi:10.1017/ S0033583508004678
16. Michel B, Boubakri H, Baharoglu Z, LeMasson M, Lestini R (2007) Recombination proteins and rescue of arrested replication forks. DNA Repair 6:967-980. doi:10.1016/j.dnarep.2007. 02.016 (Pubitemid 46880477)
17. Cano DA, Pucciarelli MG, Garcia-del Portillo F, Casadesus J (2002) Role of the RecBCD recombination pathway in Salmonella virulence. J Bacteriol 184:592-595. doi:10.1128/JB.184.2. 592-595.2002 (Pubitemid 34027404)
18. Loughlin MF, Barnard FM, Jenkins D, Sharples GJ, Jenks PJ (2003) Helicobacter pylori mutants defective in RuvC Holliday junction resolvase display reduced macrophage survival and spontaneous clearance from the murine gastric mucosa. Infect Immun 71:2022-2031. doi:10.1128/IAI.71.4.2022-2031.2003 (Pubitemid 36368736)
19. Su LY, Willner DL, Segall AM (2010) An antimicrobial peptide that targets DNA repair intermediates in vitro inhibits Salmonella growth within murine macrophages. Antimicrob Agents Chemother 54:1888-1899. doi:10.1128/AAC.01610-09
20. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 46: 3-26 (Pubitemid 33653411)
21. Lipinski CA (2000) Drug-like properties and the causes of poor solubility and poor permeability. J Pharmacol Toxicol Methods 44: 235-249 (Pubitemid 32239479)
22. Pinilla C, Appel JR, Borras E, Houghten RA (2003) Advances in the use of synthetic combinatorial chemistry: mixture-based libraries. Nat Med 9:118-122. doi:10.1038/nm0103-118 (Pubitemid 36098272)
23. Nefzi A, Ostresh JM, Giulianotti M, Houghten RA (1999) Solidphase synthesis of trisubstituted 2-imidazolidones and 2-imidazolidinethiones. J Comb Chem 1:195-198. doi:10.1021/cc980019m
24. Hensler ME, Bernstein G, Nizet V, Nefzi A (2006) Pyrrolidine biscyclic guanidines with antimicrobial activity against drug-resistant Gram-positive pathogens identified from amixture-based combinatorial library. Bioorg Med Chem Lett 16:5073-5079. doi:10. 1016/j.bmcl.2006.07.037 (Pubitemid 44247706)
25. Houghten RA, Pinilla C, Appel JR, Blondelle SE, Dooley CT, Eichler J, Nefzi A, Ostresh JM (1999) Mixture-based synthetic combinatorial libraries. J Med Chem 42:3743-3778. doi:0.1021/jm990174v (Pubitemid 29453457)
26. Ranjit DK, Rideout MC, Nefzi A, Ostresh JM, Pinilla C, SegallAM (2010) Small molecule functional analogs of peptides that inhibit lambda site-specific recombination and bind Holliday junctions. Bioorg Med Chem Lett. doi:10.1016/j.bmcl.2010.06.029
27. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
28. Ferraro MJ (2000) National committee for clinical laboratory standards methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: approved standard. NCCLS, Wayne
29. Pinilla C, Appel JR, Blanc P, Houghten RA (1992) Rapid identification of high affinity peptide ligands using positional scanning synthetic peptide combinatorial libraries. Biotechniques 13:901-905
30. Houghten RA, Pinilla C, Giulianotti MA, Appel JR, Dooley CT, Nefzi A, Ostresh JM, Yu Y, Maggiora GM, Medina-Franco JL, Brunner D, Schneider J (2008) Strategies for the use of mixturebased synthetic combinatorial libraries: scaffold ranking, direct testing in vivo, and enhanced deconvolution by computational methods. J Comb Chem 10:3-19. doi:10.1021/cc7001205
31. Boldt JL (2006) Second generation small molecule inhibitors of lambda recombination with enhanced antimicrobial activity. M.S. Thesis, San Diego State University
32. Rudolph CJ, Upton AL, Briggs GS, Lloyd RG (2010) Is RecG a general guardian of the bacterial genome?. DNA Repair 9:210-223. doi:10.1016/j.dnarep. 2009.12.014
33. WhitbyMC, Lloyd RG (1998) Targeting Holliday junctions by the RecG branch migration protein of Escherichia coli. J Biol Chem 273:19729-19739. doi:10.1074/jbc.273.31.19729 (Pubitemid 28367032)
34. Ranjit DK (2004) Small molecules that inhibit recombination and bacterial growth. Dissertation, San Diego State University
35. McKinney SA, Declais AC, Lilley DM, Ha T (2003) Structural dynamics of individual Holliday junctions. Nat Struct Biol 10:93-97. doi:10.1038/nsb883 (Pubitemid 36177087)
36. Ranjit DK, Rideout MC, Nefzi A, Ostresh JM, Pinilla C, Segall AM (2010) Small molecule functional analogs of peptides that inhibit lambda site-specific recombination and bind Holliday junctions. Bioorg Med Chem Lett 20:4531-4534. doi:10.1016/j.bmcl.2010.06.029
37. Ghosh K, Lau CK, Guo F, Segall AM, Van Duyne GD (2005) Peptide trapping of theHolliday junction intermediate inCre-loxP sitespecific recombination. J Biol Chem 280:8290-8299. doi:10.1074/ jbc.M411668200 (Pubitemid 40349731)
38. Declais AC, Lilley DM (2000) Extensive central disruption of a four-way junction on binding Cce1 resolving enzyme. J Mol Biol 296:421-433. doi:10.1006/jmbi.1999.3479
39. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63. doi:10.1016/0022-1759(83)90303-4 (Pubitemid 14203433)
40. Pan PS, Curtis FA, Carroll CL, Medina I, Liotta LA, Sharples GJ, McAlpine SR (2006) Novel antibiotics: C-2 symmetrical macrocycles inhibiting Holliday junction DNA binding by E. coli RuvC. BioorgMed Chem 14:4731-4739. doi:10.1016/j.bmc.2006.03.028 (Pubitemid 43767111)
41. Bolla ML, Azevedo EV, Smith JM, Taylor RE, Ranjit DK, Segall AM, McAlpine SR (2003) Novel antibiotics: macrocyclic peptides designed to trap Holliday junctions. Org Lett 5:109-112. doi:10. 1021/ol020204f (Pubitemid 37141197)
42. Slocum SL, Buss JA, Kimura Y, Bianco PR (2007) Characterization of the ATPase activity of the Escherichia coli RecG protein reveals that the preferred cofactor is negatively supercoiled DNA. J Mol Biol 367:647-664. doi:10.1016/j.jmb.2007.01.007 (Pubitemid 46330372)