Rapid synthesis, RNA binding, and antibacterial screening of a peptidic-aminosugar (PA) library

ACS Chemical Biology

Volumn 10, Issue 5, 2015, Pages 1278-1289

  Jiang, Liuwei ^a   Watkins, Derrick ^b   Jin, Yi ^a   Gong, Changjun ^a   King, Ada ^b   Washington, Arren Z ^c   Green, Keith D ^d   Garneau Tsodikova, Sylvie ^d   Oyelere, Adegboyega K ^c   Arya, Dev P ^a,b  

^a CLEMSON UNIVERSITY   (United States)

^b NUBAD LLC   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d University of Kentucky   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOSUGAR; NEOMYCIN; PEPTIDE; ANTIINFECTIVE AGENT; PEPTIDE LIBRARY; RNA;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CHEMICAL STRUCTURE; CONJUGATE; DRUG PROTEIN BINDING; ENZYME ACTIVITY; ESCHERICHIA COLI; GROWTH INHIBITION; NONHUMAN; PEPTIDE LIBRARY; PRIORITY JOURNAL; RNA BINDING; SOLID PHASE SYNTHESIS; STRUCTURE ACTIVITY RELATION; SYNTHESIS; BACTERIUM; CARBOHYDRATE ANALYSIS; CHEMISTRY; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SCREENING; METABOLISM; MICROBIAL SENSITIVITY TEST; MOLECULAR GENETICS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

AMINO SUGARS; ANTI-BACTERIAL AGENTS; BACTERIA; CARBOHYDRATE SEQUENCE; HIGH-THROUGHPUT SCREENING ASSAYS; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; RNA; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84930010423     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb5010367     Document Type: Article

References (60)

1. Houghton, J. L., Green, K. D., Chen, W., and Garneau-Tsodikova, S. (2010) The Future of Aminoglycosides: the End or Renaissance? ChemBioChem. 11, 880-902
2. Yang, L. and Ye, X. (2010) Development of aminoglycoside antibiotics effective against resistant bacterial strains Curr. Top. Med. Chem. 10, 1898-1826
3. Moazed, D. and Noller, H. F. (1987) Interaction of antibiotics with functional sites in 16S ribosomal RNA Nature 327, 389-394
4. Purohit, P. and Stern, S. (1994) Interactions of a small RNA with antibiotic and RNA ligands of the 30S subunit Nature 370, 659-662
5. Fourmy, D., Recht, M. I., Blanchard, S. C., and Puglisi, J. D. (1996) Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic Science 274, 1367-1371
6. Tor, Y. (2006) The ribosomal A-site as an inspiration for the design of RNA binders Biochimie 88, 1045-1051
7. Chambers, H. F. and DeLeo, F. R. (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era Nat. Rev. Microbiol. 7, 629-641
8. Bera, S., Zhanel, G. G., and Schweizer, F. (2010) Evaluation of amphiphilic aminoglycoside-peptide triazole conjugates as antibacterial agents Bioorg. Med. Chem. Lett. 20, 3031-3035
9. Bera, S., Zhanel, G. G., and Schweizer, F. (2010) Antibacterial activities of aminoglycoside antibiotic-derived cationic amphiphiles: Polyol-modified neomycin B-, kanamycin A-, amikacin-, and neamine-based amphiphiles with potent broad spectrum antibacterial activity J. Med. Chem. 53, 3626-3631
10. Findlay, B., Zhanel, G. G., and Schweizer, F. (2012) Neomycin-phenolic conjugates: polycationic amphiphiles with broad-spectrum antibacterial activity, low hemolytic activity and weak serum protein binding Bioorg. Med. Chem. Lett. 22, 1499-1503
11. Zhang, J., Chiang, F. I., Wu, L., Czyryca, P. G., Li, D., and Chang, C. T. (2008) Surprising Alteration of Antibacterial Activity of 5″-Modified Neomycin against Resistant Bacteria J. Med. Chem. 51, 7563-7573
12. Fridman, M., Belakhov, V., Yaron, S., and Baasov, T. (2003) A new class of branched aminoglycosides: pseudo-pentasaccharide derivatives of neomycin B Org. Lett. 5, 3575-3578
13. Hainrichson, M., Pokrovskaya, V., Shallom-Shezifi, D., Fridman, M., Belakhov, V., Shachar, D., Yaron, S., and Baasov, T. (2005) Branched aminoglycosides: biochemical studies and antibacterial activity of neomycin B derivatives Biorg. Med. Chem. 13, 5797-5807
14. Sitaram, N. and Nagaraj, R. (1999) Interaction of antimicrobial peptides with biological and model membranes: structural and charge requirements for activity Biochim. Biophys. Acta 1462, 29-54
15. Dathe, M. and Wieprecht, T. (1999) Structural features of helical antimicrobial peptides: their potential to modulate activity on model membranes and biological cells Biochim. Biophys. Acta 1462, 71-87
16. Hancock, R. E. W. and Rozek, A. (2002) Role of membranes in the activities of antimicrobial cationic peptides FEMS Microbiol. Lett. 206, 143-149
17. Fosso, M. Y., Li, Y., and Garneau-Tsodikova, S. (2014) New trends in aminoglycosides use MedChemComm 5, 1075-1091
18. Kumar, S., Spano, M. N., and Arya, D. P. (2013) Shape readout of AT rich DNA by carbohydrates Biopolymers 101, 720-732
19. Hamilton, P. L. and Arya, D. P. (2012) Natural product DNA major groove binders Nat. Prod. Rep. 29, 134-143
20. Xi, H., Davis, E., Ranjan, N., Xue, L., Hyde-Volpe, D., and Arya, D. P. (2011) Thermodynamics of nucleic Acid ″shape readout″ by an aminosugar Biochemistry 50, 9088-9113
21. Willis, B. and Arya, D. P. (2006) An expanding view of aminoglycoside-nucleic acid recognition Adv. Carbohydr. Chem. Biochem. 60, 251-302
22. Bera, S., Zhanel, G. G., and Schweizer, F. (2008) Design, synthesis, and antibacterial activities of neomycin-lipid conjugates: polycationic lipids with potent Gram-positive activity J. Med. Chem. 51, 6160-6164
23. Bera, S., Zhanel, G. G., and Schweizer, F. (2010) Antibacterial activity of guanidinylated neomycin B- and kanamycin A-derived amphiphilic lipid conjugates J. Antimicrob. Chemother. 65, 1224-1227
24. Bera, S., Zhanel, G. G., and Schweizer, F. (2011) Synthesis and antibacterial activity of amphiphilic lysine-ligated neomycin B conjugates Carbohydr. Res. 346, 560-568
25. Kumar, S. and Arya, D. P. (2011) Recognition of HIV TAR RNA by triazole linked neomycin dimers Bioorg. Med. Chem. Lett. 21, 4788-4792
26. Xue, L., Ranjan, N., and Arya, D. P. (2011) Synthesis and spectroscopic studies of the (neomycin)-perylene conjugate binding to human telomeric DNA Biochemistry 50, 2838-2849
27. Willis, B. and Arya, D. P. (2010) Triple recognition of B-DNA by a neomycin-Hoechst 33258-pyrene conjugate Biochemistry 49, 452-469
28. Xue, L., Xi, H., Kumar, S., Gray, D., Davis, E., Hamilton, P., Skriba, M., and Arya, D. P. (2010) Probing the recognition surface of a DNA triplex: binding studies with intercalator-neomycin conjugates Biochemistry 49, 5540-5552
29. Shaw, N. N., Xi, H., and Arya, D. P. (2008) Molecular recognition of a DNA:RNA hybrid: sub-nanomolar binding by a neomycin-methidium conjugate Bioorg. Med. Chem. Lett. 18, 4142-4145
30. Willis, B. and Arya, D. P. (2006) Recognition of B-DNA by neomycin-Hoechst 33258 conjugates Biochemistry 45, 10217-10232
31. Charles, I. and Arya, D. P. (2005) Synthesis of neomycin-DNA/peptide nucleic acid conjugates J. Carbohydr. Chem. 24, 145-160
32. Arya, D. P., Coffee, R. L., Jr., and Xue, L. (2004) From triplex to B-form duplex stabilization: reversal of target selectivity by aminoglycoside dimers Bioorg. Med. Chem. Lett. 14, 4643-4646
33. Arya, D. P. and Willis, B. (2003) Reaching into the major groove of B-DNA: synthesis and nucleic acid binding of a neomycin-hoechst 33258 conjugate J. Am. Chem. Soc. 125, 12398-12399
34. Arya, D. P., Xue, L., and Tennant, P. (2003) Combining the best in triplex recognition: synthesis and nucleic acid binding of a BQQ-neomycin conjugate J. Am. Chem. Soc. 125, 8070-8071
35. Coin, I., Beyermann, M., and Bienert, M. (2007) Solid-phase peptide synthesis: from standard procedures to the synthesis of difficult sequences Nat. Protoc. 2, 3247-3256
36. Michael, K., Wang, H., and Tor, Y. (1999) Enhanced RNA binding of dimerized aminoglycosides Biorg. Med. Chem. 7, 1361-1371
37. Boer, J., Blount, K. F., Luedtke, N. W., Elson-Schwab, L., and Tor, Y. (2005) RNA-selective modification by a platinum(II) complex conjugated to amino- and guanidinoglycosides Angew. Chem., Int. Ed. 44, 927-932
38. Quader, S., Boyd, S. E., Jenkins, I. D., and Houston, T. A. (2007) Multi-site modification of neomycin B: combined mitsunobu and click chemistry approach J. Org. Chem. 72, 1962-1979
39. Kumar, S., Kellish, P., Robinson, W. E., Wang, D., Appella, D. H., and Arya, D. P. (2012) Click dimers to target HIV TAR RNA conformation Biochemistry 51, 2331-2347
40. Watkins, D., Norris, F. A., Kumar, S., and Arya, D. P. (2013) A fluorescence-based screen for ribosome binding antibiotics Anal. Biochem. 434, 300-307
41. Zhao, F., Zhao, Q., Blount, K., Han, Q., Tor, Y., and Hermann, T. (2005) Molecular recognition of RNA by neomycin and a restricted neomycin derivative Angew. Chem., Int. Ed. 44, 5329-5334
42. Ryu, D. and Rando, R. (2001) Aminoglycoside binding to human and bacterial A-site rRNA decoding region constructs Bioorg. Med. Chem. 9, 2601-2608
43. De La Fuente, R., Sonawane, N. D., Arumainayagam, D., and Verkman, A. S. (2006) Small molecules with antimicrobial activity against E. coli and P. aeruginosa identified by high-throughput screening Br. J. Pharmacol. 149, 551-559
44. King, A., Watkins, D., Kumar, S., Ranjan, N., Gong, C., Whitlock, J., and Arya, D. P. (2013) Characterization of ribosomal binding and antibacterial activities using two orthogonal high-throughput screens Antimicrob. Agents Chemother. 57, 4717-4726
45. Shaul, P., Green, K. D., Rutenberg, R., Kramer, M., Berkov-Zrihen, Y., Breiner-Goldstein, E., Garneau-Tsodikova, S., and Fridman, M. (2011) Assessment of 6′- and 6′-N-acylation of aminoglycosides as a strategy to overcome bacterial resistance Org. Biomol. Chem. 9, 4057-4063
46. Sucheck, S. J., Wong, A. L., Koeller, K. M., Boehr, D. D., Draker, K. -., Sears, P., Wright, G. D., and Wong, C. (2000) Design of Bifunctional Antibiotics that Target Bacterial rRNA and Inhibit Resistance-Causing Enzymes J. Am. Chem. Soc. 122, 5230-5231
47. Chen, W., Biswas, T., Porter, V. R., Tsodikov, O. V., and Garneau-Tsodikova, S. (2011) Unusual regioversatility of acetyltransferase Eis, a cause of drug resistance in XDR-TB Proc. Natl. Acad. Sci. U. S. A., Early Ed. 1-5, 5
48. Green, K. D., Chen, W., Houghton, J. L., Fridman, M., and Garneau-Tsodikova, S. (2010) Exploring the substrate promiscuity of drug-modifying enzymes for the chemoenzymatic generation of N-acylated aminoglycosides ChemBioChem 11, 119-126
49. Green, K. D., Chen, W., and Garneau-Tsodikova, S. (2011) Effects of altering aminoglycoside structures on bacterial resistance enzyme activities Antimicrob. Agents Chemother. 55, 3207-3213
50. Daigle, D. M., Hughes, D. W., and Wright, G. D. (1999) Prodigious substrate specificity of AAC(6′)-APH(2″), an aminoglycoside antibiotic resistance determinant in enterococci and staphylococci Chem. Biol. 6, 99-110
51. Ogle, J. M., Brodersen, D. E., Clemons, W. M., Jr., Tarry, M. J., Carter, A. P., and Ramakrishnan, V. (2001) Recognition of cognate transfer RNA by the 30s ribosomal subunit Science 292, 897-902
52. Lynch, S. R. and Puglisi, J. D. (2001) Structural Origins of Aminoglycoside Specificity for Prokaryotic Ribosomes J. Mol. Biol. 306, 1037-1058
53. Barbieri, C. M., Kaul, M., Bozza-Hingos, M., Zhao, F., Tor, Y., Hermann, T., and Pilch, D. S. (2007) Defining the molecular forces that determine the impact of neomycin on bacterial protein synthesis: importance of the 2′-amino functionality Antimicrob. Agents Chemother. 51, 1760-1769
54. Barbieri, C. M., Kaul, M., and Pilch, D. S. (2007) Use of 2-aminopurine as a fluorescent tool for characterizing antibiotic recognition of the bacterial rRNA A-site Tetrahedron 63, 3567-6574
55. Cudic, M., Lockatell, C. V., Johnson, D. E., and L, O., Jr (2003) In vitro and in vivo activity of an antibacterial peptide analog against uropathogens Peptides 24, 807-820
56. Trott, O. and Olson, A. J. (2010) AutoDock Vina: Improving the Speed and Accuracy of Docking with a New Scoring Function, Efficient Optimization, and Multithreading J. Comput. Chem. 31, 455-461
57. Sanner, M. F. (1999) Python: a programming language for software integration and development J. Mol. Graphics & Modelling 17, 57-61
58. Brunger, A., Adams, P., Clore, G., DeLano, W., Gros, P., Grosse-Kunstleve, R., Jiang, J., Kuszewski, J., Nilges, M., Pannu, N., Read, R., Rice, L., Simonson, T., and Warren, G. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921
59. Pratt, S.-D., David, C.-A., Black-Schaefer, C., Dandliker, P.-J., Xuei, X., Warrior, U., Burns, D.-J., Zhong, P., Cao, Z., Saiki, A.-Y., Lerner, C.-G., Chovan, L.-E., Soni, N.-B., Nilius, A.-M., Wagenaar, F.-L., Merta, P.-J., Traphagen, L.-M., and Beutel, B.-A. (2004) A strategy for discovery of novel broad-spectrum antibacterials using a highthroughput Streptococcus pneumoniae transcription/translation screen J. Biomol Screen. 9, 3-11
60. Thorne, C.-A., Lafleur, B., Lewis, M., Hanson, A.-J., Jernigan, K.-K., Weaver, D.-C., Huppert, K.-A., Chen, T.-W., Wichaidit, C., Cselenyi, C.-S., Tahinci, E., Meyers, K.-C., Waskow, E., Orton, D., Salic, A., Lee, L.-A., Robbins, D.-J., Huppert, S.-S., and Lee, E. (2011) A biochemical screen for identification of small-molecule regulators of the Wnt pathway using Xenopus egg extracts J. Biomol. Scr. 16, 995-1006