Impact of Ribosomal Modification on the Binding of the Antibiotic Telithromycin Using a Combined Grand Canonical Monte Carlo/Molecular Dynamics Simulation Approach

PLoS Computational Biology

Volumn 9, Issue 6, 2013, Pages

  Small, Meagan C ^a   Lopes, Pedro ^a   Andrade, Rodrigo B ^b   MacKerell, Alexander D ^a  

^a UNIVERSITY OF MARYLAND   (United States)

^b Temple University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; ANTIBIOTICS; BINDING ENERGY; ENTROPY; ESCHERICHIA COLI; METABOLITES; METHYLATION; MONTE CARLO METHODS;

BINDING-SITES; DYNAMICS SIMULATION; E. COLI; GRAND-CANONICAL MONTE CARLO; MACROLIDE ANTIBIOTICS; MACROLIDES; METHYLTRANSFERASES; SIMULATION APPROACH; TELITHROMYCIN; WILD TYPES;

MOLECULAR DYNAMICS;

TELITHROMYCIN; WATER;

ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CELL INTERACTION; CONTROLLED STUDY; DRUG BINDING SITE; DRUG STRUCTURE; ENTROPY; GENE DELETION; GENE INSERTION; GENE MUTATION; GENE REARRANGEMENT; GRAND CANONICAL MONTE CARLO METHOD; HYDROGEN BOND; MOLECULAR DYNAMICS; MONTE CARLO METHOD; RIBOSOME; WILD TYPE;

EID: 84879524541     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003113     Document Type: Article

References (96)

1. Wright GD, (2011) Molecular mechanisms of antibiotic resistance. Chem Commun (Camb) 47: 4055-4061.
2. Poehlsgaard J, Douthwaite S, (2005) The bacterial ribosome as a target for antibiotics. Nat Rev Microbiol 3: 870-881.
3. Tenson T, Mankin A, (2006) Antibiotics and the ribosome. Mol Microbiol 59: 1664-1677.
4. Brandi L, Marzi S, Fabbretti A, Fleishcer C, Hill W, et al. (2004) The translation initiation functions of IF2: targets for thiostrepton inhibition. J Mol Biol 335: 881-894.
5. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, et al. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407: 340-348.
6. Fourmy D, Recht MI, Blanchard SC, Puglisi JD, (1996) Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274: 1367-1371.
7. Ganoza MC, Kiel MC, (2001) A ribosomal ATPase is a target for hygromycin B inhibition on Escherichia coli ribosomes. Antimicrob Agents Chemother 45: 2813-2819.
8. Hansen JL, Ippolito JA, Ban N, Nissen P, Moore PB, et al. (2002) The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol Cell 10: 117-128.
9. Rodnina MV, Stark H, Savelsbergh A, Wieden HJ, Mohr D, et al. (2000) GTPases mechanisms and functions of translation factors on the ribosome. Biol Chem 381: 377-387.
10. Schlunzen F, Zarivach R, Harms J, Bashan A, Tocilj A, et al. (2001) Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 413: 814-821.
11. Kirillov S, Porse BT, Vester B, Woolley P, Garrett RA, (1997) Movement of the 3′-end of tRNA through the peptidyl transferase centre and its inhibition by antibiotics. FEBS Lett 406: 223-233.
12. Tenson T, Lovmar M, Ehrenberg M, (2003) The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome. J Mol Biol 330: 1005-1014.
13. Douthwaite S, (2001) Structure-activity relationships of ketolides vs. macrolides. Clin Microbiol Infect 7 Suppl 3: 11-17.
14. Katz L, Ashley GW, (2005) Translation and protein synthesis: macrolides. Chem Rev 105: 499-528.
15. Tu D, Blaha G, Moore PB, Steitz TA, (2005) Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121: 257-270.
16. Vester B, Douthwaite S, (2001) Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob Agents Chemother 45: 1-12.
17. Weisblum B, (1995) Insights into erythromycin action from studies of its activity as inducer of resistance. Antimicrob Agents Chemother 39: 797-805.
18. Weisblum B, (1995) Erythromycin resistance by ribosome modification. Antimicrob Agents Chemother 39: 577-585.
19. Denoya C, Dubnau D, (1989) Mono- and dimethylating activities and kinetic studies of the ermC 23 S rRNA methyltransferase. J Biol Chem 264: 2615-2624.
20. Nielsen AK, Douthwaite S, Vester B, (1999) Negative in vitro selection identifies the rRNA recognition motif for ErmE methyltransferase. Rna 5: 1034-1041.
21. Zhong P, Pratt SD, Edalji RP, Walter KA, Holzman TF, et al. (1995) Substrate requirements for ErmC' methyltransferase activity. J Bacteriol 177: 4327-4332.
22. Champney WS, Tober CL, (2001) Structure-activity relationships for six ketolide antibiotics. Curr Microbiol 42: 203-210.
23. Liu M, Douthwaite S, (2002) Activity of the ketolide telithromycin is refractory to Erm monomethylation of bacterial rRNA. Antimicrob Agents Chemother 46: 1629-1633.
24. Pfister P, Jenni S, Poehlsgaard J, Thomas A, Douthwaite S, et al. (2004) The structural basis of macrolide-ribosome binding assessed using mutagenesis of 23S rRNA positions 2058 and 2059. J Mol Biol 342: 1569-1581.
25. Douthwaite S, Jalava J, Jakobsen L, (2005) Ketolide resistance in Streptococcus pyogenes correlates with the degree of rRNA dimethylation by Erm. Mol Microbiol 58: 613-622.
26. Berisio R, Harms J, Schluenzen F, Zarivach R, Hansen HA, et al. (2003) Structural insight into the antibiotic action of telithromycin against resistant mutants. J Bacteriol 185: 4276-4279.
27. Douthwaite S, Hansen LH, Mauvais P, (2000) Macrolide-ketolide inhibition of MLS-resistant ribosomes is improved by alternative drug interaction with domain II of 23S rRNA. Mol Microbiol 36: 183-193.
28. Hansen LH, Mauvais P, Douthwaite S, (1999) The macrolide-ketolide antibiotic binding site is formed by structures in domains II and V of 23S ribosomal RNA. Mol Microbiol 31: 623-631.
29. Bonnefoy A, Girard AM, Agouridas C, Chantot JF, (1997) Ketolides lack inducibility properties of MLS(B) resistance phenotype. J Antimicrob Chemother 40: 85-90.
30. Champney WS, Chittum HS, Tober CL, (2003) A 50S ribosomal subunit precursor particle is a substrate for the ErmC methyltransferase in Staphylococcus aureus cells. Curr Microbiol 46: 453-460.
31. Dubnau D, (1984) Translational attenuation: the regulation of bacterial resistance to the macrolide-lincosamide-streptogramin B antibiotics. CRC Crit Rev Biochem 16: 103-132.
32. Lai CJ, Weisblum B, (1971) Altered methylation of ribosomal RNA in an erythromycin-resistant strain of Staphylococcus aureus. Proc Natl Acad Sci U S A 68: 856-860.
33. Usary J, Champney WS, (2001) Erythromycin inhibition of 50S ribosomal subunit formation in Escherichia coli cells. Mol Microbiol 40: 951-962.
34. Wolter N, Smith AM, Farrell DJ, Northwood JB, Douthwaite S, et al. (2008) Telithromycin resistance in Streptococcus pneumoniae is conferred by a deletion in the leader sequence of erm(B) that increases rRNA methylation. Antimicrob Agents Chemother 52: 435-440.
35. Bryskier A, (2000) Ketolides-telithromycin, an example of a new class of antibacterial agents. Clin Microbiol Infect 6: 661-669.
36. Salyers AA, Amabile-Cuevas CF, (1997) Why are antibiotic resistance genes so resistant to elimination? Antimicrob Agents Chemother 41: 2321-2325.
37. Shoemaker NB, Vlamakis H, Hayes K, Salyers AA, (2001) Evidence for extensive resistance gene transfer among Bacteroides spp. and among Bacteroides and other genera in the human colon. Appl Environ Microbiol 67: 561-568.
38. Dunkle JA, Xiong L, Mankin AS, Cate JH, (2010) Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc Natl Acad Sci U S A 107: 17152-17157.
39. Bulkley D, Innis CA, Blaha G, Steitz TA, (2010) Revisiting the structures of several antibiotics bound to the bacterial ribosome. Proc Natl Acad Sci U S A 107: 17158-17163.
40. Metropolis N, Rosenbluth AW, Rosenbluth MN, (1953) Equation of state calculations by fast computing machines. J Chem Phys 21: 1087-1092.
41. Barnett-Norris J, Guarnieri F, Hurst DP, Reggio PH, (1998) Exploration of biologically relevant conformations of anandamide, 2-arachidonylglycerol, and their analogues using conformational memories. J Med Chem 41: 4861-4872.
42. Guarnieri F, Still W, (1994) A rapidly convergent simulation method: Mixed Monte Carlo/stochastic dynamics. J Comput Chem 15: 1302-1310.
43. Guarnieri F, Weinstein H, (1996) Conformational Memories and the Exploration of biologically relevant peptide conformations: an illustration for the gonadotropin-releasing hormone. J Am Chem Soc 118: 5580-5589.
44. Mezei M, (1980) A cavity-biased (T, V, mu) Monte Carlo method for the computer simulation of fluids. Mol Phys 40: 901-906.
45. Mezei M, (1987) Grand-canonical ensemble Monte Carlo study of dense liquid. Mol Phys 61: 565-582.
46. Erratum (1989) 67: 1207-1208.
47. Resat H, Mezei M, (1994) Grand Canonical Monte Carlo Simulation of Water Positions in Crystal Hydrates. J Am Chem Soc 116: 7451-7452.
48. Resat H, Mezei M, (1996) Grand canonical ensemble Monte Carlo simulation of the dCpG/proflavine crystal hydrate. Biophys J 71: 1179-1190.
49. Resat H, Mezei M, McCammon JA, (1996) Use of the Grand Canonical Ensemble in Potential of Mean Force Calculations. J PHys Chem 100: 1426-1433.
50. Whitnell RM, Hurst DP, Reggio PH, Guarnieri F, (2008) Conformational memories with variable bond lengths. J Comput Chem 29: 741-752.
51. Deng Y, Roux B, (2008) Computation of binding free energy with molecular dynamics and grand canonical Monte Carlo simulations. J Chem Phys 128: 1-8.
52. Woo HJ, Dinner AR, Roux B, (2004) Grand canonical Monte Carlo simulations of water in protein environments. J Chem Phys 121: 6392-6400.
53. Ge X, Roux B, (2010) Calculation of the standard binding free energy of sparsomycin to the ribosomal peptidyl-transferase P-site using molecular dynamics simulations with restraining potentials. J Mol Recognit 23: 128-141.
54. Ge X, Roux B, (2010) Absolute binding free energy calculations of sparsomycin analogs to the bacterial ribosome. J Phys Chem B 114: 9525-9539.
55. Baker CM, Anisimov VM, MacKerell AD Jr, (2011) Development of CHARMM polarizable force field for nucleic acid bases based on the classical Drude oscillator model. The journal of physical chemistry B 115: 580-596.
56. Vester B, Hansen LH, Douthwaite S, (1995) The conformation of 23S rRNA nucleotide A2058 determines its recognition by the ErmE methyltransferase. Rna 1: 501-509.
57. Villsen ID, Vester B, Douthwaite S, (1999) ErmE methyltransferase recognizes features of the primary and secondary structure in a motif within domain V of 23 S rRNA. J Mol Biol 286: 365-374.
58. LeTourneau N, Vimal P, Klepacki D, Mankin A, Melman A, (2012) Synthesis and antibacterial activity of desosamine-modified macrolide derivatives. Bioorg Med Chem Lett 22: 4575-4578.
59. Kostopoulou ON, Petropoulos AD, Dinos GP, Choli-Papadopoulou T, Kalpaxis DL, (2012) Investigating the entire course of telithromycin binding to Escherichia coli ribosomes. Nucleic Acids Res 40: 5078-5087.
60. Llano-Sotelo B, Dunkle J, Klepacki D, Zhang W, Fernandes P, et al. (2010) Binding and action of CEM-101, a new fluoroketolide antibiotic that inhibits protein synthesis. Antimicrob Agents Chemother 54: 4961-4970.
61. Denis A, Bretin F, Fromentin C, Bonnet A, Piltan G, et al. (2000) Beta-keto-ester chemistry and ketolides. Synthesis and antibacterial activity of 2-halogeno, 2-methyl and 2,3 enol-ether ketolides. Bioorg Med Chem Lett 10: 2019-2022.
62. Brooks BR, Brooks CL III, Mackerell AD Jr, Nilsson L, Petrella RJ, et al. (2009) CHARMM: the biomolecular simulation program. J Comput Chem 30: 1545-1614.
63. MacKerell AD Jr, Bashford DBM, Dunbrack RL Jr, Evanseck JD, Field MJ, et al. (1998) All-atom empirical potential for molecular modeling and dynamic studies of protein. J Phys Chem B 102: 3586-3616.
64. Mackerell AD Jr, Feig M, Brooks CL III, (2004) Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25: 1400-1415.
65. MacKerell AD Jr, Feig M, Brooks CL III, (2004) Improved treatment of the protein backbone in empirical force fields. J Am Chem Soc 126: 698-699.
66. Denning EJ, Priyakumar UD, Nilsson L, Mackerell AD Jr, (2012) Impact of 2′-hydroxyl sampling on the conformational properties of RNA: update of the CHARMM all-atom additive force field for RNA. J Comput Chem 32: 1929-1943.
67. Foloppe N, MacKerell AD Jr, (2000) All-atom empirical force field for nucleic acids: 1) Parameter optimization based on small molecule and condensed phase macromolecular target data. J Comp Chem 21: 86-104.
68. Hart K, Foloppe N, Baker CM, Denning EJ, Nilsson L, et al. (2012) Optimization of the CHARMM additive force field for DNA: Improved treatment of the BI/BII conformational equilibrium. J Chem Theory Comput 8: 348-362.
69. MacKerell AD Jr, Banavali N, Foloppe N, (2000) Development and current status of the CHARMM force field for nucleic acids. Biopolymers 56: 257-265.
70. Guvench O, Greene SN, Kamath G, Brady JW, Venable RM, et al. (2008) Additive empirical force field for hexopyranose monosaccharides. J Comput Chem 29: 2543-2564.
71. Guvench O, Hatcher ER, Venable RM, Pastor RW, Mackerell AD Jr, (2009) CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses. J Chem Theory Comput 5: 2353-2370.
72. Guvench O, Mallajosyula SS, Raman EP, Hatcher E, Vanommeslaeghe K, et al. (2011) CHARMM additive all-atom force field for carbohydrate derivatives and its utility in polysaccharide and carbohydrate-protein modeling. J Chem Theory Comput 7: 3162-3180.
73. Hatcher E, Guvench O, Mackerell AD Jr, (2009) CHARMM Additive All-Atom Force Field for Acyclic Polyalcohols, Acyclic Carbohydrates and Inositol. J Chem Theory Comput 5: 1315-1327.
74. Hatcher E, Guvench O, Mackerell AD Jr, (2009) CHARMM additive all-atom force field for aldopentofuranoses, methyl-aldopentofuranosides, and fructofuranose. J Phys Chem B 113: 12466-12476.
75. Raman EP, Guvench O, MacKerell AD Jr, (2010) CHARMM additive all-atom force field for glycosidic linkages in carbohydrates involving furanoses. J Phys Chem B 114: 12981-12994.
76. Vanommeslaeghe K, Hatcher E, Acharya C, Kundu S, Zhong S, et al. (2010) CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. J Comput Chem 31: 671-690.
77. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML, (1983) Comparison of Simple Potential Functions for Simulating Liquid Water. Journal of Chemical Physics 79: 926-935.
78. Vanommeslaeghe K, MacKerell AD Jr, (2012) Automation of the CHARMM General Force Field (CGenFF) I: bond perception and atom typing. J Chem Inf Model 52: 3144-3154.
79. Vanommeslaeghe K, Raman EP, MacKerell AD Jr, (2012) Automation of the CHARMM General Force Field (CGenFF) II: assignment of bonded parameters and partial atomic charges. J Chem Inf Model 52: 3155-3168.
80. Beglov D, Roux B, (1994) Finite representation of an infinite bulk system: solvent boundary potential for computer simulations. J Chem Phys 100: 9050-9063.
81. Brooks CL III, Brunger A, Karplus M, (1985) Active site dynamics in protein molecules: a stochastic boundary molecular-dynamics approach. Biopolymers 24: 843-865.
82. Brooks CL III, Karplus M, (1983) Deformably stochastic boundaries in molecular dynamics. J Chem Phys 79: 6312-6325.
83. Brooks CL III, Karplus M, (1989) Solvent effects on protein motion and protein effects on solvent motion. Dynamics of the active site region of lysozyme. J Mol Biol 208: 159-181.
84. Brunger A, Brooks CL III, Karplus M, (1984) Stochastic boundary conditions for molecular dynamics simulations of ST2 water. Chem Phys Lett 105: 495-500.
85. Deng Y, Roux B, (2004) Hydration of amino acid side chains: nonpolar and electrostatic contributions calculated from staged molecular dynamics free energy simulations with explicit water molecules. J Phys Chem B 108: 16567-16576.
86. van Gunsteren WF, Karplus M, (1980) A Method for Constrained Energy Minimization of Macromolecules. Journal of Computational Chemistry 1: 266-274.
87. Hu J, Ma A, Dinner AR, (2006) Monte Carlo simulations of biomolecules: The MC module in CHARMM. J Comput Chem 27: 203-216.
88. Im W, Berneche S, Roux B, (2001) Generalized solvent boundary potential for computer simulations. J Chem Phys 114: 2924-2937.
89. Lynch GC, Pettitt BM, (2000) Semi-grand canonical molecular dynamics simulation of bovine pancreatic trypsin inhibitor. Chem Phys 258: 405-413.
90. Langevin P, (1908) Sur la theorie du mouvement brownien. C R Acad Sci (Paris) 146: 530-533.
91. Lemons DS, Gythiel A, (1997) Paul Langevin's 1908 paper "On the theory of brownian moetion" ["Sur la theorie du mouvement brownien," C.R. Acad. Sci. (Paris) 146, 530-533 (1908)]. Am J Phys 65: 1079-1081.
92. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
93. Ryckaert J-P, Ciccotti G, Berendsen HJC, (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23.
94. Allen MP, Tildesley DJ (1987) Computer Simulation of Liquids. Oxford: Clarendon Press. 385 p.
95. Steinbach PJ, Brooks BR, (1994) New Spherical-Cutoff Methods of Long-Range Forces in Macromolecular Simulations. J Comp Chem 15: 667-683.
96. De Loof H, Nilsson L, Rigler R, (1992) Molecular dynamics simulation of galanin in aqueous and nonaqueous solution. J Am Chem Soc 114: 4028-4035.