Synergy of streptogramin antibiotics occurs independently of their effects on translation

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 9, 2014, Pages 5269-5279

  Noeske, Jonas ^a   Huang, Jian ^b   Olivier, Nelson B ^b   Giacobbe, Robert A ^b   Zambrowski, Mark ^b   Cate, Jamie H D ^a  

^a University of California Berkeley   (United States)

^b ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DALFOPRISTIN; DALFOPRISTIN PLUS QUINUPRISTIN; DEPSIPEPTIDE; FLOPRISTIN; LINOPRISTIN; MIKAMYCIN B; NXL 103; QUINUPRISTIN; UNCLASSIFIED DRUG; VIRGINIAMYCIN M; VIRGINIAMYCIN S; ANTIINFECTIVE AGENT; DRUG COMBINATION; FLOPRISTIN, LINOPRISTIN DRUG COMBINATION; STREPTOGRAMIN DERIVATIVE; VIRGINIAMYCIN;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC SENSITIVITY; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOASSAY; CHECKERBOARD ASSAY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEINOCOCCUS RADIODURANS; DISSOCIATION CONSTANT; DRUG BINDING; DRUG POTENTIATION; DRUG STRUCTURE; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; HALOARCULA MARISMORTUI; HELICOBACTER PYLORI; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; ISOTHERMAL TITRATION CALORIMETRY; LARGE RIBOSOMAL SUBUNIT; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; RIBOSOME; RNA TRANSLATION; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES; TRANSCRIPTION COUPLED TRANSLATION ASSAY; WILD TYPE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; DRUG COMBINATION; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST; PROTEIN SYNTHESIS; ULTRASTRUCTURE;

ANTI-BACTERIAL AGENTS; CRYSTALLOGRAPHY, X-RAY; DRUG COMBINATIONS; DRUG SYNERGISM; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; MICROBIAL SENSITIVITY TESTS; PROTEIN BIOSYNTHESIS; RIBOSOMES; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STREPTOGRAMIN A; STREPTOGRAMIN B; STREPTOGRAMINS; VIRGINIAMYCIN;

EID: 84906077400     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.03389-14     Document Type: Article

References (46)

1. Centers for Disease Control and Prevention. 2013. Antibiotic resistance threats in the United States. Threat report 2013. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/drugresistance/threat-report- 2013/.
2. Donadio S, Maffioli S, Monciardini P, Sosio M, Jabes D. 2010. Antibiotic discovery in the twenty-first century: current trends and future perspectives. J. Antibiot. (Tokyo) 63:423-430. http://dx.doi.org/10.1038/ja.2010.62.
3. Wilson DN. 2014. Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat. Rev. Microbiol. 12:35-48. http://dx.doi.org/10.1038/ nrmicro3155.
4. Yates JD, Schaible PJ. 1962. Virginiamycin as an antibiotic for poultry feeds. Nature 194:183-184. http://dx.doi.org/10.1038/194183b0.
5. Pfizer. 2013. Synercid I.V. (quinupristin and dalfopristin for injection), Pfizer Inc., New York, NY. http://labeling.pfizer.com/ShowLabeling. aspx?id=712.
6. Dupuis M, Leclercq R. 2006. Activity of a new oral streptogramin, XRP2868, against Gram-positive cocci harboring various mechanisms of resistance to streptogramins. Antimicrob. Agents Chemother. 50:237-242. http://dx.doi.org/10.1128/AAC.50.1.237-242.2006. (Pubitemid 43042927)
7. Eliopoulos GM, Ferraro MJ, Wennersten CB, Moellering RC, Jr. 2005. In vitro activity of an oral streptogramin antimicrobial, XRP2868, against Gram-positive bacteria. Antimicrob. Agents Chemother. 49:3034-3039. http://dx.doi.org/10.1128/AAC.49.7.3034-3039.2005. (Pubitemid 40917636)
8. Goldstein EJ, Citron DM, Merriam CV, Warren YA, Tyrrell KL, Fernandez HT, Bryskier A. 2005. Comparative in vitro activities of XRP 2868, pristinamycin, quinupristin-dalfopristin, vancomycin, daptomycin, linezolid, clarithromycin, telithromycin, clindamycin, and ampicillin against anaerobic Gram-positive species, actinomycetes, and lactobacilli. Antimicrob. Agents Chemother. 49:408-413. http://dx.doi.org/10.1128/AAC.49.1.408-413.2005.
9. Mabe S, Champney WS. 2005. A comparison of a new oral streptogramin XRP 2868 with quinupristin-dalfopristin against antibiotic-resistant strains of Haemophilus influenzae, Staphylococcus aureus, and Streptococcus pneumoniae. Curr. Microbiol. 51:363-366. http://dx.doi.org/10.1007/s00284-005-0027-9. (Pubitemid 41759131)
10. Politano AD, Sawyer RG. 2010. NXL-103, a combination of flopristin and linopristin, for the potential treatment of bacterial infections including community-acquired pneumonia and MRSA. Curr. Opin. Investig. Drugs 11:225-236.
11. Delgado G, Jr, Neuhauser MM, Bearden DT, Danziger LH. 2000. Quinupristin-dalfopristin: an overview. Pharmacotherapy 20:1469-1485. http://dx.doi.org/10.1592/phco.20.19.1469.34858.
12. Vazquez D. 1966. Studies on the mode of action of the streptogramin antibiotics. J. Gen. Microbiol. 42:93-106. http://dx.doi.org/10.1099/00221287- 42-1-93.
13. Bouanchaud DH. 1992. In-vitro and in-vivo synergic activity and fractional inhibitory concentration (FIC) of the components of a semisynthetic streptogramin, RP 59500. J. Antimicrob. Chemother. 30(Suppl A):95-99.
14. Cocito C. 1979. Antibiotics of the virginiamycin family, inhibitors which contain synergistic components. Microbiol. Rev. 43:145-192.
15. Neu HC, Chin NX, Gu JW. 1992. The in-vitro activity of new streptogramins, RP 59500, RP 57669 and RP 54476, alone and in combination. J. Antimicrob. Chemother. 30(Suppl A):83-94.
16. Chinali G, Nyssen E, Di Giambattista M, Cocito C. 1988. Action of erythromycin and virginiamycin S on polypeptide synthesis in cell-free systems. Biochim. Biophys. Acta 951:42-52. http://dx.doi.org/10.1016/0167-4781(88)90023- 1. (Pubitemid 18265226)
17. Chinali G, Nyssen E, Di Giambattista M, Cocito C. 1988. Inhibition of polypeptide synthesis in cell-free systems by virginiamycin S and erythromycin. Evidence for a common mode of action of type B synergimycins and 14-membered macrolides. Biochim. Biophys. Acta 949:71-78. (Pubitemid 18026114)
18. Pestka S. 1977. Molecular mechanisms of protein biosynthesis. Academic Press, New York, NY.
19. Cocito C, Vanlinden F. 1983. Inhibitory action of virginiamycin components on cell-free systems for polypeptide formation from Bacillus subtilis. Arch. Microbiol. 135:8-11. http://dx.doi.org/10.1007/BF00419474. (Pubitemid 13033528)
20. Contreras A, Vázquez D. 1977. Synergistic interaction of the streptogramins with the ribosome. Eur. J. Biochem. 74:549-551. http://dx.doi.org/10.1111/j.1432-1033.1977.tb11423.x. (Pubitemid 8080076)
21. Parfait R, de Béthune MP, Cocito C. 1978. A spectrofluorimetric study of the interaction between virginiamycin S and bacterial ribosomes. Mol. Gen. Genet. 166:45-51. http://dx.doi.org/10.1007/BF00379728. (Pubitemid 9047092)
22. Hansen JL, Moore PB, Steitz TA. 2003. Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J. Mol. Biol. 330:1061-1075.http://dx.doi.org/10.1016/S0022-2836(03)00668-5. (Pubitemid 36818903)
23. Harms JM, Schlünzen F, Fucini P, Bartels H, Yonath A. 2004. Alterations at the peptidyl transferase centre of the ribosome induced by the synergistic action of the streptogramins dalfopristin and quinupristin. BMC Biol. 2:4. http://dx.doi.org/10.1186/1741-7007-2-4.
24. 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. http://dx.doi.org/10.1016/j.cell.2005.02.005. (Pubitemid 40546393)
25. Hsieh MH, Yu CM, Yu VL, Chow JW. 1993. Synergy assessed by checkerboard. A critical analysis. Diagn. Microbiol. Infect. Dis. 16:343-349. http://dx.doi.org/10.1016/0732-8893(93)90087-N. (Pubitemid 23146839)
26. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 Å resolution. Science 310:827-834. http://dx.doi.org/10.1126/science.1117230. (Pubitemid 41567336)
27. Zhang W, Dunkle JA, Cate JH. 2009. Structures of the ribosome in intermediate states of ratcheting. Science 325:1014-1017. http://dx.doi.org/10. 1126/science.1175275.
28. Kabsch W. 2010. XDS. Acta Cryst. 66:125-132. http://dx.doi.org/10.1107/ S0907444909047337.
29. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66:213-221. http://dx.doi.org/10.1107/S0907444909052925.
30. Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60:2126-2132. http://dx.doi.org/10.1107/S0907444904019158. (Pubitemid 41742764)
31. CLSI. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard - 9th ed. CLSI document M07-A9. Clinical and Laboratory Standards Institute, Wayne, PA.
32. CLSI. 2013. Performance standards for antimicrobial susceptibility testing; 23rd informational supplement. CLSI document M100-S23. Clinical and Laboratory Standards Institute, Wayne, PA.
33. Pillai SK, Moellering RC, Jr, Eliopoulos GM. 2005. Antimicrobial combinations, p 365-440. In Lorian V (ed), Antibiotics in laboratory medicine, 5th ed. Lipincott Williams & Wilkins, Philadelphia, PA.
34. Meletiadis J, Pournaras S, Roilides E, Walsh TJ. 2010. Defining fractional inhibitory concentration index cutoffs for additive interactions based on self-drug additive combinations, Monte Carlo simulation analysis, and in vitro-in vivo correlation data for antifungal drug combinations against Aspergillus fumigatus. Antimicrob. Agents Chemother. 54:602-609. http://dx.doi.org/10.1128/AAC.00999-09.
35. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1. http://dx.doi.org/10.1093/jac/ dkg301. (Pubitemid 36850074)
36. Brosius J, Ullrich A, Raker MA, Gray A, Dull TJ, Gutell RR, Noller HF. 1981. Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal RNA operon of E. coli. Plasmid 6:112-118. http://dx.doi.org/10.1016/ 0147-619X(81)90058-5. (Pubitemid 11001952)
37. Buurman ET, Foulk MA, Gao N, Laganas VA, McKinney DC, Moustakas DT, Rose JA, Shapiro AB, Fleming PR. 2012. Novel rapidly diversifiable antimicrobial RNA polymerase switch region inhibitors with confirmed mode of action in Haemophilus influenzae. J. Bacteriol. 194:5504-5512. http://dx.doi.org/10.1128/JB.01103-12.
38. Pankuch GA, Kelly LM, Lin G, Bryskier A, Couturier C, Jacobs MR, Appelbaum PC. 2003. Activities of a new oral streptogramin, XRP 2868, compared to those of other agents against Streptococcus pneumoniae and Haemophilus species. Antimicrob. Agents Chemother. 47:3270-3274. http://dx.doi.org/10.1128/ AAC.47.10.3270-3274.2003. (Pubitemid 37229588)
39. Mukhtar TA, Wright GD. 2005. Streptogramins, oxazolidinones, and other inhibitors of bacterial protein synthesis. Chem. Rev. 105:529-542. http://dx.doi.org/10.1021/cr030110z. (Pubitemid 40351632)
40. Depardieu F, Courvalin P. 2001. Mutation in 23S rRNA responsible for resistance to 16-membered macrolides and streptogramins in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 45:319-323. http://dx.doi.org/10.1128/ AAC.45.1.319-323.2001. (Pubitemid 32039137)
41. Wang G, Taylor DE. 1998. Site-specific mutations in the 23S rRNA gene of Helicobacter pylori confer two types of resistance to macrolide-lincosamide- streptogramin B antibiotics. Antimicrob. Agents Chemother. 42:1952-1958. (Pubitemid 28363075)
42. Sigmund CD, Ettayebi M, Morgan EA. 1984. Antibiotic resistance mutations in 16S and 23S ribosomal RNA genes of Escherichia coli. Nucleic Acids Res. 12:4653-4663. http://dx.doi.org/10.1093/nar/12.11.4653.
43. Cocito C, Di Giambattista M, Nyssen E, Vannuffel P. 1997. Inhibition of protein synthesis by streptogramins and related antibiotics. J. Antimicrob. Chemother. 39(Suppl A):7-13. (Pubitemid 27281493)
44. Singh KV, Weinstock GM, Murray BE. 2002. An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin. Antimicrob. Agents Chemother. 46:1845-1850. http://dx.doi.org/10.1128/AAC.46.6.1845-1850.2002. (Pubitemid 34535206)
45. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289:905-920. http://dx.doi.org/10.1126/science.289.5481.905. (Pubitemid 30659939)
46. Churchill CD, Navarro-Whyte L, Rutledge LR, Wetmore SD. 2009. Effects of the biological backbone on DNA-protein stacking interactions: the interplay between the backbone⋯π and π⋯π components. Phys. Chem. Chem. Phys. 11:10657-10670. http://dx.doi.org/10.1039/b910747a.