A fluorescence-based screen for ribosome binding antibiotics

Analytical Biochemistry

Volumn 434, Issue 2, 2013, Pages 300-307

  Watkins, Derrick ^a   Norris, F A ^a,b   Kumar, Sunil ^b   Arya, Dev P ^b  

^a NUBAD LLC   (United States)

^b CLEMSON UNIVERSITY   (United States)

Author keywords

A site; Aminoglycoside; F neo; Fluorescence; Ribosome binding ligands; Ribosome RNA; Screening

Indexed keywords

ANTIBIOTICS; BINDING ENERGY; DIGITAL LIBRARIES; ESCHERICHIA COLI; FLUORESCENCE; PROBES; SCREENING;

A-SITE; AMINOGLYCOSIDES; BACTERIAL RIBOSOMES; ELECTROSTATIC ENVIRONMENTS; HIGH-THROUGHPUT SCREENS; LIQUID HANDLING ROBOTS; RELATIVE BINDING AFFINITY; RIBOSOME BINDING;

MACROMOLECULES;

NEOMYCIN; RNA;

ANISOTROPY; ARTICLE; BINDING AFFINITY; DRUG BINDING; DRUG BINDING SITE; ESCHERICHIA COLI; FLUORESCENCE ANALYSIS; NONHUMAN; PRIORITY JOURNAL; RIBOSOME;

EID: 84873377396     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2012.12.003     Document Type: Article

References (65)

1. C.S. Chow, and F.M. Bogdan A structural basis for RNA-ligand interactions Chem. Rev. 97 1997 1489 1514
2. D.P. Arya Aminoglycoside-nucleic acid interactions: the case for neomycin Top. Curr. Chem. 253 2005 149 178
3. A. Schatz, E. Bugie, and S.A. Waksman Streptomycin, a substance exhibiting antibiotic activity against Gram-positive and Gram-negative bacteria Proc. Soc. Exp. Biol. Med. 55 1944 66 69
4. S.A. Waksman, and H.A. Lechevalier Neomycin, a new antibiotic active against streptomycin-resistant bacteria, including tuberculosis organisms J. Antibiot. 109 1949 305 309
5. D.P. Arya Aminoglycoside Antibiotics: From Chemical Biology to Drug Discovery 2007 Wiley-Interscience Hoboken, NJ
6. S.R. Lynch, and J.D. Puglisi Structural origins of aminoglycoside specificity for prokaryotic ribosomes J. Mol. Biol. 306 2001 1037 1058
7. E.A. De Stasio, D. Moazed, H.F. Noller, and A.E. Dahlberg Mutations in 16S ribosomal RNA disrupt antibiotic-RNA interactions EMBO J. 8 1989 1213 1216
8. J. Zhou, G. Wang, L.H. Zhang, and X.S. Ye Modifications of aminoglycoside antibiotics targeting RNA Med. Res. Rev. 27 2007 279 316
9. J. Davies, and G.D. Wright Bacterial resistance to aminoglycoside antibiotics Trends Microbiol. 5 1997 234 240
10. A. Beauclerk, and E. Cundliffe Sites of action of two ribosomal-RNA methylases responsible for resistance to aminoglycosides J. Mol. Biol. 193 1987 661 671
11. M. Mingeot-Leclercq, Y. Glupczynski, and P. Tulkens Aminoglycosides: activity and resistance Antimicrob. Agents Chemother. 43 1999 727 737
12. Y. Zhou, V.E. Gregor, B.K. Ayida, G.C. Winters, Z. Sun, D. Murphy, G. Haley, D. Bailey, J.M. Froelich, S. Fish, S.E. Webber, T. Hermann, and D. Wall Synthesis and SAR of 3,5-diamino-piperidine derivatives: novel antibacterial translation inhibitors as aminoglycoside mimetics Bioorg. Med. Chem. Lett. 17 2007 1206 1210
13. M.C. Bryan, and C.-H. Wong Aminoglycoside array for the high-throughput analysis of small molecule-RNA interactions Tetrahedron Lett. 45 2004 3639 3642
14. S. Kumar, P. Kellish, W.E. Robinson Jr., D. Wang, D.H. Appella, and D.P. Arya Click dimers to target HIV TAR RNA conformation Biochemistry 51 2012 2331 2347
15. L. Yu, T.K. Oost, J.M. Schkeryantz, J. Yang, D. Janowick, and S.W. Fesik Discovery of aminoglycoside mimetics by NMR-based screening of Escherichia coli A-site RNA J. Am. Chem. Soc. 125 2003 4444 4450
16. D. Fourmy, M.I. Recht, S.C. Blanchard, and J.D. Puglisi Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic Science 274 1996 1367 1371
17. D. Fourmy, M.I. Recht, and J.D. Puglisi Binding of neomycin-class aminoglycoside antibiotics to the A-site of 16S rRNA J. Mol. Biol. 277 1998 347 362
18. M.I. Recht, D. Fourmy, S.C. Blanchard, K.D. Dahlquist, and J.D. Puglisi RNA sequence determinants for aminoglycoside binding to an A-site rRNA model oligonucleotide J. Mol. Biol. 262 1996 421 436
19. F. Zhao, Q. Zhao, K. Blount, Q. Han, Y. Tor, and T. Hermann Molecular recognition of RNA by neomycin and a restricted neomycin derivative Angew. Chem. Int. Ed. 44 2005 5329 5334
20. W.K.C. Park, M. Auer, H. Jaksche, and C.-H. Wong Rapid combinatorial synthesis of aminoglycoside antibiotic mimetics: use of a polyethylene glycol-linked amine and a neamine-derived aldehyde in multiple component condensation as a strategy for the discovery of new inhibitors of the HIV RNA Rev responsive element J. Am. Chem. Soc. 118 1996 10150 10155
21. H. Xi, E. Davis, N. Ranjan, L. Xue, D. Hyde-Volpe, and D.P. Arya Thermodynamics of nucleic acid "shape readout" by an aminosugar Biochemistry 50 2011 9088 9113
22. O. Trott, and A.J. Olson AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading J. Comput. Chem. 31 2010 455 461
23. A. Pedretti, L. Villa, and G. Vistoli VEGA - an open platform to develop chemo-bio-informatics applications, using plug-in architecture and script programming J. Comput. Aided Mol. Des. 18 2004 167 173
24. M.F. Sanner Python: a programming language for software integration and development J. Mol. Graphics Modell. 17 1999 57 61
25. A. Brunger, P. Adams, G. Clore, W. DeLano, P. Gros, R. Grosse-Kunstleve, J. Jiang, J. Kuszewski, M. Nilges, N. Pannu, R. Read, L. Rice, T. Simonson, and G. Warren Crystallography and NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D 54 1998 905 921
26. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: application to microtubules and the ribosome Proc. Natl. Acad. Sci. USA 98 2001 10037 10041
27. T.J. Dolinsky, P. Czodrowski, H. Li, J.E. Nielsen, J.H. Jensen, G. Klebe, and N.A. Baker PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res. 35 2007 W522 W525
28. T.J. Dolinsky, J.E. Nielsen, J.A. McCammon, and N.A. Baker PDB2PQR: an automated pipeline for the setup, execution, and analysis of Poisson-Boltzmann electrostatics calculations Nucleic Acids Res. 32 2004 W665 W667
29. a of fluorescein to optimize binding assays Anal. Chem. 79 2007 6775 6782
30. a shift of a fluorophore Eur. J. Biochem. 173 1988 227 231
31. J. Alvarez-Pez, L. Ballesteros, E. Talavera, and J. Yguerabide Fluorescein excited-state proton exchange reactions: nanosecond emission kinetics and correlation with steady-state fluorescence intensity J. Phys. Chem. 105 2001 6320 6332
32. a shift of a fluorophore: 2. Transfer RNA Eur. J. Biochem. 173 1988 233 239
33. J.P. Knemeyer, N. Marme, and M. Sauer Probes for detection of specific DNA sequences at the single-molecule level Anal. Chem. 72 2000 3717 3724
34. S.A. Marras, F.R. Kramer, and S. Tyagi Efficiencies of fluorescence resonance energy transfer and contact-mediated quenching in oligonucleotide probes Nucleic Acids Res. 30 2002 e122
35. R.T. Ranasinghe, and T. Brown Fluorescence based strategies for genetic analysis Chem. Commun. 44 2005 5487 5502
36. R. Sjoback, J. Nygren, and M. Kubista Characterization of fluorescein-oligonucleotide conjugates and measurement of local electrostatic potential Biopolymers 46 1998 445 453
37. K. Hamasaki, and R.R. Rando Specific binding of aminoglycosides to a human rRNA construct based on a DNA polymorphism which causes aminoglycoside-induced deafness Biochemistry 36 1997 12323 12328
38. D. Ryu, and R. Rando Aminoglycoside binding to human and bacterial A-site rRNA decoding region constructs Bioorg. Med. Chem. 9 2001 2601 2608
39. H. Diehl, and N. Horchak-Morris Studies on fluorescein. 5. The absorbency of fluorescein in the ultraviolet, as a function of pH Talanta 34 1987 739 741
40. a shift of a fluorophore. 1. The 3′ terminus of 16S RNA Eur. J. Biochem. 173 1988 227 231
41. B. Llano-Sotelo, E.F. Azucena, L.P. Kotra, S. Mobashery, and C.S. Chow Aminoglycosides modified by resistance enzymes display diminished binding to the bacterial ribosomal aminoacyl-tRNA site Chem. Biol. 9 2002 455 463
42. F. Liang, W.A. Greenberg, J.A. Hammond, J. Hoffmann, S.R. Head, and C. Wong Evaluation of RNA-binding specificity of aminoglycosides with DNA microarrays Proc. Natl. Acad. Sci. USA 103 2006 12311 12316
43. M. Kaul, C.M. Barbieri, and D.S. Pilch Fluorescence-based approach for detecting and characterizing antibiotic-induced conformational changes in ribosomal RNA: comparing aminoglycoside binding to prokaryotic and eukaryotic ribosomal RNA sequences J. Am. Chem. Soc. 126 2004 3447 3453
44. Y. Xie, A.V. Dix, and Y. Tor FRET enabled real time detection of RNA-small molecule binding J. Am. Chem. Soc. 131 2009 17605 17614
45. Y. Wang, and R.R. Rando Specific binding of aminoglycoside antibiotics to RNA Chem. Biol. 2 1995 281 290
46. Y. Wang, J. Killian, K. Hamasaki, and R.R. Rando RNA molecules that specifically and stoichiometrically bind aminoglycoside antibiotics with high affinities Biochemistry 35 1996 12338 12346
47. Y. Wang, K. Hamasaki, and R.R. Rando Specificity of aminoglycoside binding to RNA constructs derived from the 16S rRNA decoding region and the HIV-RRE activator region Biochemistry 36 1997 768 779
48. D.H. Ryu, A. Litovchick, and R.R. Rando Stereospecificity of aminoglycoside-ribosomal interactions Biochemistry 41 2002 10499 10509
49. J.H. Zhang, T.D. Chung, and K.R. Oldenburg A simple statistical parameter for use in evaluation and validation of high throughput screening assays J. Biomol. Screen. 4 1999 67 73
50. K.D. Grimes, and C.C. Aldrich A high-throughput screening fluorescence polarization assay for fatty acid adenylating enzymes in Mycobacterium tuberculosis Anal. Biochem. 417 2011 264 273
51. S. Duffy, and V.M. Avery Development and optimization of a novel 384-well anti-malarial imaging assay validated for high-throughput screening Am. J. Trop. Med. Hyg. 86 2012 84 92
52. M.M. Morelock, E.A. Hunter, T.J. Moran, S. Heynen, C. Laris, M. Thieleking, M. Akong, I. Mikic, S. Callaway, R.P. DeLeon, A. Goodacre, D. Zacharias, and J.H. Price Statistics of assay validation in high throughput cell imaging of nuclear factor kappa B nuclear translocation Assay Drug Dev. Technol. 3 2005 483 499
53. B. Willis, and D.P. Arya An expanding view of aminoglycoside-nucleic acid recognition Adv. Carbohydr. Chem. Biochem. 60 2006 251 302
54. N.N. Shaw, H. Xi, and D.P. Arya Molecular recognition of a DNA:RNA hybrid: sub-nanomolar binding by a neomycin-methidium conjugate Bioorg. Med. Chem. Lett. 18 2008 4142 4145
55. B. Willis, and D.P. Arya Major groove recognition of DNA by carbohydrates Curr. Org. Chem. 10 2006 663 673
56. B. Willis, and D.P. Arya Recognition of B-DNA by neomycin-Hoechst 33258 conjugates Biochemistry 45 2006 10217 10232
57. N. Ranjan, K.F. Andreasen, S. Kumar, D. Hyde-Volpe, and D.P. Arya Aminoglycoside binding to Oxytricha nova telomeric DNA Biochemistry 49 2010 9891 9903
58. B. Willis, and D.P. Arya Triple recognition of B-DNA by a neomycin-Hoechst 33258-pyrene conjugate Biochemistry 49 2010 452 469
59. L. Xue, N. Ranjan, and D.P. Arya Synthesis and spectroscopic studies of the aminoglycoside (neomycin)-perylene conjugate binding to human telomeric DNA Biochemisry 50 2011 2838 2849
60. S. Kumar, L. Xue, and D.P. Arya Neomycin-neomycin dimer: an all-carbohydrate scaffold with high affinity for AT-rich DNA duplexes J. Am. Chem. Soc. 133 2011 7361 7375
61. K. Hamasaki, and R.R. Rando A high-throughput fluorescence screen to monitor the specific binding of antagonists to RNA targets Anal. Biochem. 261 1998 183 190
62. P.L. Tran, E. Largy, F. Hamon, M.P. Teulade-Fichou, and J.L. Mergny Fluorescence intercalator displacement assay for screening G4 ligands towards a variety of G-quadruplex structures Biochimie 93 2011 1288 1296
63. D. Boger, B. Fink, and M. Hedrick Total synthesis of distamycin A and 2640 analogues: a solution-phase combinatorial approach to the discovery of new, bioactive DNA binding agents and development of a rapid, high-throughput screen for determining relative DNA binding affinity or DNA binding sequence selectivity J. Am. Chem. Soc. 122 2000 6382 6394
64. L.S. Glass, A. Bapat, M.R. Kelley, M.M. Georgiadis, and E.C. Long Semi-automated high-throughput fluorescent intercalator displacement-based discovery of cytotoxic DNA binding agents from a large compound library Bioorg. Med. Chem. Lett. 20 2010 1685 1688
65. E. Largy, F. Hamon, and M.P. Teulade-Fichou Development of a high-throughput G4-FID assay for screening and evaluation of small molecules binding quadruplex nucleic acid structures Anal. Bioanal. Chem. 400 2011 3419 3427