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Structural and energetic comparison of the complexes of aminoglycosides with the model of the ribosomal A-site. (English) Zbl 1357.92026
Summary: 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 \(\Delta\)G with the total charge had the coefficient of determination \(R^{2}\) over \(0.8-0.9\), depending on experimental data set, and was the highest of all descriptors.

92C40 Biochemistry, molecular biology
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[1] P.B. Alper, M. Hendrix, P. Sears and C.-H. Wong, Probing the Specificity of Aminoglycoside-Ribosomal RNA Interactions with Designed Synthetic Analogs. J. Am. Chem. Soc.120 (1998) 1965-1978. · doi:10.1021/ja972599h
[2] C.M. Barbieri, A.R. Srinivasan and D.S. Pilch, 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:10.1021/ja0457516
[3] H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov and P.E. Bourne, The protein data bank. Nucleic Acids Res.28 (2000) 235-242. · Zbl 05434923 · doi:10.1093/nar/28.1.235
[4] K.F. Blount and Y. Tor, Using pyrene-labeled HIV-1 TAR to measure RNA-small molecule binding. Nucleic Acids Res.31 (2003) 5490-5500. · doi:10.1093/nar/gkg755
[5] 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.
[6] S.-Y. Chen and T.-H. Lin, 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:10.1002/jmr.1008
[7] K. Darty, A. Denise and Y. Ponty, VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinform.25 (2009) 1974-1975. · Zbl 05744129 · doi:10.1093/bioinformatics/btp250
[8] N. Demeshkina, L. Jenner, E. Westhof, M. Yusupov and G. Yusupova, A new understanding of the decoding principle on the ribosome. Nature484 (2012) 256-259. · doi:10.1038/nature10913
[9] M. Długosz and J. Trylska, Aminoglycoside Association Pathways with the 30S Ribosomal Subunit. J. Phys. Chem. B113 (2009) 7322-7330. · doi:10.1021/jp8112914
[10] M. Długosz, J.M. Antosiewicz and J. Trylska, Association of Aminoglycosidic Antibiotics with the Ribosomal A-Site Studied with Brownian Dynamics. J. Chem. Theory Comput.4 (2008) 549-559. · doi:10.1021/ct700210n
[11] M. Dudek, J. Romanowska, T. Wituła and J. Trylska, Interactions of amikacin with the RNA model of the ribosomal A-site: computational, spectroscopic and calorimetric studies. Biochimie102 (2014) 188-202. · doi:10.1016/j.biochi.2014.03.009
[12] B. François, J. Szychowski, S.S. Adhikari, K. Pachamuthu, E.E. Swayze, R.H. Griffey, M.T. Migawa, E. Westhof and S. Hanessian, Antibacterial Aminoglycosides with a Modified Mode of Binding to the Ribosomal-RNA Decoding Site. Angew. Chem., Int. Ed.43 (2004) 6735-6738. · doi:10.1002/anie.200462092
[13] B. François, R.J. Russell, J.B. Murray, F. Aboul-ela, B. Masquida, Q. Vicens and E. Westhof, 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:10.1093/nar/gki862
[14] A. Górska, M. Jasiński and J. Trylska, MINT: software to identify motifs and short-range interactions in trajectories of nucleic acids. Nucl. Acids Res.43 (2015) e114. · doi:10.1093/nar/gkv559
[15] S. Hobbie, P. Pfister, C. Bruell, E. Westhof and E. Boettger, Analysis of the contribution of individual substituents in 4,6-aminoglycoside-ribosome interaction. Antimicrob. Agents Chemother.49 (2005) 5112-5118. · doi:10.1128/AAC.49.12.5112-5118.2005
[16] B. Honig and A. Nicholls, Classical electrostatics in biology and chemistry. Science268 (1995) 1144-1149. · doi:10.1126/science.7761829
[17] J.L. Houghton, K.D. Green, W. Chen and S. Garneau-Tsodikova, The future of aminoglycosides: the end or renaissance? Chem. Bio. Chem.11 (2010) 880-902. · doi:10.1002/cbic.200900779
[18] W. Humphrey, A. Dalke and K. Schulten, VMD - Visual Molecular Dynamics. J. Mol. Graph.14 (1996) 33-38. · doi:10.1016/0263-7855(96)00018-5
[19] A. Jakalian, B.L. Bush, D.B. Jack and C.I. Bayly, Fast, efficient generation of high-quality atomic charges. AM1-BCC model: I. Method. J. Comput. Chem.21 (2000) 132-146. · Zbl 05428621 · doi:10.1002/(SICI)1096-987X(20000130)21:2<132::AID-JCC5>3.0.CO;2-P
[20] S. Jana and J. Deb, Molecular understanding of aminoglycoside action and resistance. Appl. Microbiol. Biotechnol.70 (2006) 140-150. · doi:10.1007/s00253-005-0279-0
[21] M. Kaul and D.S. Pilch, Thermodynamics of Aminoglycoside-rRNA Recognition: The Binding of Neomycin-Class Aminoglycosides to the A Site of 16S rRNA. Biochemistry41 (2002) 7695-7706. · doi:10.1021/bi020130f
[22] M. Kaul, C.M. Barbieri, J.E. Kerrigan and D.S. Pilch, 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:10.1016/S0022-2836(02)01452-3
[23] M. Kaul, C.M. Barbieri and D.S. Pilch, 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:10.1016/j.jmb.2004.11.041
[24] S. Kevin, Energy landscape of the ribosomal decoding center. Biochimie88 (2006) 1053-1059. · doi:10.1016/j.biochi.2006.06.012
[25] J. Kondo, B. François, R.J. Russell, J.B. Murray and E. Westhof, Crystal structure of the bacterial ribosomal decoding site complexed with amikacin containing the gamma-amino-alpha-hydroxybutyryl (haba) group. Biochimie88 (2006) 1027-1031. · doi:10.1016/j.biochi.2006.05.017
[26] J. Kondo, M. Koganei and T. Kasahara, Crystal Structure and Specific Binding Mode of Sisomicin to the Bacterial Ribosomal Decoding Site. ACS Med. Chem. Lett.3 (2012) 741-744. · doi:10.1021/ml300145y
[27] M. Kulik, A.M. Goral, M. Jasiński, P.M. Dominiak and J. Trylska, Electrostatic interactions in aminoglycoside-RNA complexes. Biophys. J.108 (2015) 655-665. · doi:10.1016/j.bpj.2014.12.020
[28] C. Ma, N.A. Baker, S. Joseph and J.A. McCammon, Binding of Aminoglycoside Antibiotics to the Small Ribosomal Subunit: A Continuum Electrostatics Investigation. J. Am. Chem. Soc.124 (2002) 1438-1442. · doi:10.1021/ja016830+
[29] S. Meroueh and S. Mobashery, 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:10.1111/j.1747-0285.2007.00505.x
[30] J. Panecka, M. Havrila, K. Réblová, J. Šponer and Joanna Trylska. 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. B118 (2014) 6687-6701. · doi:10.1021/jp5030685
[31] P. Pfister, S. Hobbie, C. Brüll, N. Corti, A. Vasella, E. Westhof and E.C. Böttger, Mutagenesis of 16S rRNA C1409-G1491 base-pair differentiates between 6’OH and 6’NH3+ aminoglycosides. J. Mol. Biol.346 (2005) 467-475. · doi:10.1016/j.jmb.2004.11.073
[32] D.S. Pilch, M. Kaul, C.M. Barbieri and J.E. Kerrigan, Thermodynamics of aminoglycoside-rRNA recognition. Biopolymers70 (2003) 58-79. · doi:10.1002/bip.10411
[33] J. Romanowska, P. Setny and J. Trylska, Molecular Dynamics Study of the Ribosomal A-Site. J. Phys. Chem. B112 (2008) 15227-15243. · doi:10.1021/jp806814s
[34] D.H. Ryu and R.R. Rando, Aminoglycoside binding to human and bacterial A-Site rRNA decoding region constructs. Bioorg. Med. Chem.9 (2001) 2601-2608. · doi:10.1016/S0968-0896(01)00034-7
[35] A.C. Vaiana, E. Westhof and P. Auffinger, A molecular dynamics simulation study of an aminoglycoside/A-site RNA complex: conformational and hydration patterns. Biochimie88 (2006) 1061-1073. · doi:10.1016/j.biochi.2006.06.006
[36] A. Vaiana and K. Sanbonmatsu, Stochastic gating and drug-ribosome interactions. J. Mol. Biol.386 (2009) 648-661. · doi:10.1016/j.jmb.2008.12.035
[37] Q. Vicens and E. Westhof, Crystal structure of paromomycin docked into the eubacterial ribosomal decoding A site. Structure9 (2001) 647-658. · doi:10.1016/S0969-2126(01)00629-3
[38] Q. Vicens and E. Westhof, 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:10.1016/S1074-5521(02)00153-9
[39] Q. Vicens and E. Westhof, Crystal structure of geneticin bound to a bacterial 16S ribosomal RNA A site oligonucleotide. J. Mol. Biol.326 (2003) 1175-1188. · doi:10.1016/S0022-2836(02)01435-3
[40] Q. Vicens and E. Westhof, Molecular recognition of aminoglycoside antibiotics by ribosomal RNA and resistance enzymes: an analysis of x-ray crystal structures. Biopolymers70 (2003) 42-57. · doi:10.1002/bip.10414
[41] H. Wang and Y. Tor, Electrostatic Interactions in RNA Aminoglycosides Binding. J. Am. Chem. Soc.119 (1997) 8734-8735. · doi:10.1021/ja9715105
[42] J. Wang, P. Cieplak and P.A. Kollman, 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. · Zbl 05429499 · doi:10.1002/1096-987X(200009)21:12<1049::AID-JCC3>3.0.CO;2-F
[43] C.-H. Wong, M. Hendrix, E.S. Priestley and W.A. Greenberg, Specificity of aminoglycoside antibiotics for the A-site of the decoding region of ribosomal RNA. Chem. Biol.5 (1998) 397-406. · doi:10.1016/S1074-5521(98)90073-4
[44] G. Yang, J. Trylska, Y. Tor and J.A. McCammon, 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:10.1021/jm060288o
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