Understanding the interactions which govern aminoglycoside antibiotic binding to ribosomal RNA is essential to propose modifications of these antibiotics. We have investigated the hydrogen bond patterns, solvent accessibility, and stacking energies of the nucleobases in twelve different aminoglycoside-RNA crystal complexes. These analyses pointed to some antibiotic-induced RNA structural differences that depend on the type of bound aminoglycoside. The largest differences were in the hydrogen bonding pattern in the vicinity of the U1406 and U1495 base pairs, especially in the complexes with geneticin and modified paromomycin. The complexes that stand out were the ones with neamine and kanamycin. We found that the solvent-accessible surface area buried upon aminoglycoside binding to RNA increases with the number of aminoglycoside rings but its correlation with the net charge of the antibiotic or experimental binding free energies was weak. We also investigated the dependence of other aminoglycoside characterizing descriptors, such as the number of rings and total charge, on the experimentally determined Gibbs energies. The correlation of with the total charge had the coefficient of determination over 0.8–0.9, depending on experimental data set, and was the highest of all descriptors.
Accepté le :
DOI : 10.1051/ro/2015041
Mots clés : Aminoglycosides, ribosomal RNA, A-site, solvent accessible surface area, hydrogen bonds, nucleobase stacking
@article{RO_2016__50_2_375_0,
author = {Kulik, Marta and Trylska, Joanna},
title = {Structural and energetic comparison of the complexes of aminoglycosides with the model of the ribosomal {A-site}},
journal = {RAIRO - Operations Research - Recherche Op\'erationnelle},
pages = {375--386},
publisher = {EDP-Sciences},
volume = {50},
number = {2},
year = {2016},
doi = {10.1051/ro/2015041},
zbl = {1357.92026},
language = {en},
url = {http://www.numdam.org/articles/10.1051/ro/2015041/}
}
TY - JOUR AU - Kulik, Marta AU - Trylska, Joanna TI - Structural and energetic comparison of the complexes of aminoglycosides with the model of the ribosomal A-site JO - RAIRO - Operations Research - Recherche Opérationnelle PY - 2016 SP - 375 EP - 386 VL - 50 IS - 2 PB - EDP-Sciences UR - http://www.numdam.org/articles/10.1051/ro/2015041/ DO - 10.1051/ro/2015041 LA - en ID - RO_2016__50_2_375_0 ER -
%0 Journal Article %A Kulik, Marta %A Trylska, Joanna %T Structural and energetic comparison of the complexes of aminoglycosides with the model of the ribosomal A-site %J RAIRO - Operations Research - Recherche Opérationnelle %D 2016 %P 375-386 %V 50 %N 2 %I EDP-Sciences %U http://www.numdam.org/articles/10.1051/ro/2015041/ %R 10.1051/ro/2015041 %G en %F RO_2016__50_2_375_0
Kulik, Marta; Trylska, Joanna. Structural and energetic comparison of the complexes of aminoglycosides with the model of the ribosomal A-site. RAIRO - Operations Research - Recherche Opérationnelle, Tome 50 (2016) no. 2, pp. 375-386. doi : 10.1051/ro/2015041. http://www.numdam.org/articles/10.1051/ro/2015041/
, , and , Probing the Specificity of Aminoglycoside-Ribosomal RNA Interactions with Designed Synthetic Analogs. J. Am. Chem. Soc. 120 (1998) 1965–1978. | DOI
, and , Deciphering the origins of observed heat capacity changes for aminoglycoside binding to prokaryotic and eukaryotic ribosomal RNA a-sites: a calorimetric, computational, and osmotic stress study. J. Am. Chem. Soc. 126 (2004) 14380–14388. | DOI
, , , , , , and , The protein data bank. Nucleic Acids Res. 28 (2000) 235–242. | DOI
and , Using pyrene-labeled HIV-1 TAR to measure RNA-small molecule binding. Nucleic Acids Res. 31 (2003) 5490–5500. | DOI
D.A. Case, T.A. Darden, T.E. Cheatham, C.L. Simmerling, J. Wang, R.E. Duke, R. Luo, M. Crowley, R.C. Walker, W. Zhang, K.M. Merz, B. Wang, S. Hayik, A. Roitberg, G. Seabra, I. Kolossváry, K.F. Wong, F. Paesani, J. Vanicek, X. Wu, S.R. Brozell, T. Steinbrecher, H. Gohlke, L. Yang, C. Tan, J. Mongan, V. Hornak, G. Cui, D.H. Mathews, M.G. Seetin, C. Sagui, V. Babin and P.A. Kollman, Amber 11. University of California, San Francisco.
and , A molecular dynamics study on binding recognition between several 4,5 and 4,6-linked aminoglycosides with A-site RNA. J. Mol. Recognit. 23 (2010) 423–434. | DOI
, and , VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinform. 25 (2009) 1974–1975. | DOI
, , , and , A new understanding of the decoding principle on the ribosome. Nature 484 (2012) 256–259. | DOI
and , Aminoglycoside Association Pathways with the 30S Ribosomal Subunit. J. Phys. Chem. B 113 (2009) 7322–7330. | DOI
, and , Association of Aminoglycosidic Antibiotics with the Ribosomal A-Site Studied with Brownian Dynamics. J. Chem. Theory Comput. 4 (2008) 549–559. | DOI
, , and , Interactions of amikacin with the RNA model of the ribosomal A-site: computational, spectroscopic and calorimetric studies. Biochimie 102 (2014) 188–202. | DOI
, , , , , , , and , Antibacterial Aminoglycosides with a Modified Mode of Binding to the Ribosomal-RNA Decoding Site. Angew. Chem., Int. Ed. 43 (2004) 6735–6738. | DOI
, , , , , and , Crystal structures of complexes between aminoglycosides and decoding a site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res. 33 (2005) 5677–5690. | DOI
, and , MINT: software to identify motifs and short-range interactions in trajectories of nucleic acids. Nucl. Acids Res. 43 (2015) e114. | DOI
, , , and , Analysis of the contribution of individual substituents in 4,6-aminoglycoside-ribosome interaction. Antimicrob. Agents Chemother. 49 (2005) 5112–5118. | DOI
and , Classical electrostatics in biology and chemistry. Science 268 (1995) 1144–1149. | DOI
, , and , The future of aminoglycosides: the end or renaissance? Chem. Bio. Chem. 11 (2010) 880–902. | DOI
, and , VMD – Visual Molecular Dynamics. J. Mol. Graph. 14 (1996) 33–38. | DOI
, , and , Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method. J. Comput. Chem. 21 (2000) 132–146. | DOI
and , Molecular understanding of aminoglycoside action and resistance. Appl. Microbiol. Biotechnol. 70 (2006) 140–150. | DOI
and , Thermodynamics of Aminoglycoside-rRNA Recognition: The Binding of Neomycin-Class Aminoglycosides to the A Site of 16S rRNA. Biochemistry 41 (2002) 7695–7706. | DOI
, , and , Coupling of Drug Protonation to the Specific Binding of Aminoglycosides to the A Site of 16S rRNA: Elucidation of the Number of Drug Amino Groups Involved and their Identities. J. Mol. Biol. 326 (2003) 1373–1387. | DOI
, and , Defining the Basis for the Specificity of Aminoglycoside-rRNA Recognition: A Comparative Study of Drug Binding to the A Sites of Escherichia coli and Human rRNA. J. Mol. Biol. 346 (2005) 119–134. | DOI
, Energy landscape of the ribosomal decoding center. Biochimie 88 (2006) 1053–1059. | DOI
, , , and , Crystal structure of the bacterial ribosomal decoding site complexed with amikacin containing the gamma-amino-alpha-hydroxybutyryl (haba) group. Biochimie 88 (2006) 1027–1031. | DOI
, and , Crystal Structure and Specific Binding Mode of Sisomicin to the Bacterial Ribosomal Decoding Site. ACS Med. Chem. Lett. 3 (2012) 741–744. | DOI
, , , and , Electrostatic interactions in aminoglycoside-RNA complexes. Biophys. J. 108 (2015) 655–665. | DOI
, , and , Binding of Aminoglycoside Antibiotics to the Small Ribosomal Subunit: A Continuum Electrostatics Investigation. J. Am. Chem. Soc. 124 (2002) 1438–1442. | DOI
and , Conformational transition in the aminoacyl t-RNA site of the bacterial ribosome both in the presence and absence of an aminoglycoside antibiotic. Chem. Biol. Drug. Des. 69 (2007) 291–297. | DOI
, , , and . Role of S-turn2 in the Structure, Dynamics, and Function of Mitochondrial Ribosomal A-Site. A Bioinformatics and Molecular Dynamics Simulation Study. J. Phys. Chem. B 118 (2014) 6687–6701. | DOI
, , , , , and , Mutagenesis of 16S rRNA C1409-G1491 base-pair differentiates between 6’OH and 6’NH3+ aminoglycosides. J. Mol. Biol. 346 (2005) 467–475. | DOI
, , and , Thermodynamics of aminoglycoside-rRNA recognition. Biopolymers 70 (2003) 58–79. | DOI
, and , Molecular Dynamics Study of the Ribosomal A-Site. J. Phys. Chem. B 112 (2008) 15227–15243. | DOI
and , Aminoglycoside binding to human and bacterial A-Site rRNA decoding region constructs. Bioorg. Med. Chem. 9 (2001) 2601–2608. | DOI
, and , A molecular dynamics simulation study of an aminoglycoside/A-site RNA complex: conformational and hydration patterns. Biochimie 88 (2006) 1061–1073. | DOI
and , Stochastic gating and drug-ribosome interactions. J. Mol. Biol. 386 (2009) 648–661. | DOI
and , Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure 9 (2001) 647–658. | DOI
and , Crystal Structure of a Complex between the Aminoglycoside Tobramycin and an Oligonucleotide Containing the Ribosomal Decoding A Site. Chem. Biol. 9 (2002) 747–755. | DOI
and , Crystal structure of geneticin bound to a bacterial 16S ribosomal RNA A site oligonucleotide. J. Mol. Biol. 326 (2003) 1175–1188. | DOI
and , Molecular recognition of aminoglycoside antibiotics by ribosomal RNA and resistance enzymes: an analysis of x-ray crystal structures. Biopolymers 70 (2003) 42–57. | DOI
and , Electrostatic Interactions in RNA Aminoglycosides Binding. J. Am. Chem. Soc. 119 (1997) 8734–8735. | DOI
, and , How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21 (2000) 1049–1074. | DOI
, , and , Specificity of aminoglycoside antibiotics for the A-site of the decoding region of ribosomal RNA. Chem. Biol. 5 (1998) 397–406. | DOI
, , and , Binding of aminoglycosidic antibiotics to the oligonucleotide A-site model and 30S ribosomal subunit: Poisson–Boltzmann model, thermal denaturation, and fluorescence studies. J. Med. Chem. 49 (2006) 5478–5490. | DOI
Cité par Sources :
