Whole-genome analyses of Enterococcus faecium isolates with diverse daptomycin MICs

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 8, 2014, Pages 4527-4534

  Diaz, Lorena ^a   Tran, Truc T ^b,c   Munita, Jose M ^b,d   Miller, William R ^b   Rincon, Sandra ^a   Carvajal, Lina P ^a   Wollam, Aye ^e   Reyes, Jinnethe ^a,b   Panesso, Diana ^a,b   Rojas, Natalia L ^a   Shamoo, Yousif ^f   Murray, Barbara E ^b   Weinstock, George M ^e,g   Ariasa, Cesar A ^a,b  

^a UNIVERSIDAD EL BOSQUE   (Colombia)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

^d UNIVERSIDAD DEL DESARROLLO   (Chile)

^e WASHINGTON UNIVERSITY   (United States)

^f RICE UNIVERSITY   (United States)

^g JACKSON LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4,4-DIFLUORO-4-BORA-3A,4A-DIAZA-S-INDACENE; AMPICILLIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; BORON DERIVATIVE; DAPTOMYCIN; FLUORESCENT DYE; VANCOMYCIN;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; BACTERIAL GENOME; CELL MEMBRANE; CELL WALL; CHEMISTRY; DRUG EFFECTS; ENTEROCOCCUS FAECIUM; GENE EXPRESSION; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; REGULATOR GENE;

AMINO ACID SUBSTITUTION; AMPICILLIN; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BORON COMPOUNDS; CELL MEMBRANE; CELL WALL; DAPTOMYCIN; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENTEROCOCCUS FAECIUM; FLUORESCENT DYES; GENE EXPRESSION; GENES, REGULATOR; GENOME, BACTERIAL; MICROBIAL SENSITIVITY TESTS; VANCOMYCIN; VANCOMYCIN RESISTANCE;

EID: 84905374570     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02686-14     Document Type: Article

References (47)

1. Galloway-Peña J, Roh JH, Latorre M, Qin X, Murray BE. 2012. Genomic and SNP analyses demonstrate a distant separation of the hospital and community-associated clades of Enterococcus faecium. PLoS One 7:e30187. http://dx.doi.org/10.1371/journal.pone.0030187.
2. Lebreton F, van Schaik W, McGuire AM, Godfrey P, Griggs A, Mazumdar V, Corander J, Cheng L, Saif S, Young S, Zeng Q, Wortman J, Birren B, Willems RJ, Earl AM, Gilmore MS. 2013. Emergence of epidemic multidrugresistant Enterococcus faecium from animal and commensal strains. mBio 4:e00534-13. http://dx.doi.org/10.1128/mBio.00534-13.
3. Arias CA, Murray BE. 2012. The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10:266-278. http://dx.doi.org/10. 1038/nrmicro2761.
4. Arias CA, Torres HA, Singh KV, Panesso D, Moore J, Wanger A, Murray BE. 2007. Failure of daptomycin monotherapy for endocarditis caused by an Enterococcus faecium strain with vancomycin-resistant and vancomycin-susceptible subpopulations and evidence of in vivo loss of the vanA gene cluster. Clin. Infect. Dis. 45:1343-1346. http://dx.doi.org/10.1086/522656.
5. Munoz-Price LS, Lolans K, Quinn JP. 2005. Emergence of resistance to daptomycin during treatment of vancomycin-resistant Enterococcus faecalis infection. Clin. Infect. Dis. 41:565-566. http://dx.doi.org/10.1086/432121.
6. Lewis JS, Owens A, Cadena J, Sabol K, Patterson JE, Jorgensen JH. 2005. Emergence of daptomycin resistance in Enterococcus faecium during daptomycin therapy. Antimicrob. Agents Chemother. 94:1664-1665.
7. Pogliano J, Pogliano N, Silverman JA. 2012. Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins. J. Bacteriol. 194:4494-4504. http://dx.doi.org/10.1128/JB. 00011-12.
8. Tran TT, Panesso D, Mishra NN, Mileykovskaya E, Guan Z, Munita JM, Reyes J, Diaz L, Weinstock GM, Murray BE, Shamoo Y, Dowhan W, Bayer AS, Arias CA. 2013. Daptomycin-resistant Enterococcus faecalis diverts the antibiotic molecule from the division septum and remodels cell membrane phospholipids. mBio 4:e00281-13. http://dx.doi.org/10.1128/mBio.00281-13.
9. Miller C, Kong J, Tran TT, Arias CA, Saxer G, Shamoo Y. 2013. Adaptation of Enterococcus faecalis to daptomycin reveals an ordered progression to resistance. Antimicrob. Agents Chemother. 57:5373-5383. http://dx.doi.org/10. 1128/AAC.01473-13.
10. Jordan S, Junker A, Helmann JD, Mascher T. 2006. Regulation of LiaRS-dependent gene expression in Bacillus subtilis: identification of inhibitor proteins, regulator binding sites, and target genes of a conserved cell envelope stress-sensing two-component system. J. Bacteriol. 188:5153-5166. http://dx.doi.org/10.1128/JB.00310-06.
11. Arias CA, Panesso D, McGrath DM, Qin X, Mojica MF, Miller C, Diaz L, Tran TT, Rincon S, Barbu EM, Reyes J, Roh JH, Lobos E, Sodergren E, Pasqualini R, Arap W, Quinn JP, Shamoo Y, Murray BE, Weinstock GM. 2011. Genetic basis for in vivo daptomycin resistance in enterococci. N. Engl. J. Med. 365:892-900. http://dx.doi.org/10.1056/NEJMoa1011138.
12. Mishra NN, Yang SJ, Sawa A, Rubio A, Nast CC, Yeaman MR, Bayer AS. 2009. Analysis of cell membrane characteristics of in vitro-selected daptomycin-resistant strains of methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 53:2312-2318. http://dx.doi.org/10.1128/AAC.01682- 08.
13. Munita JM, Tran TT, Diaz L, Panesso D, Reyes J, Murray BE, Arias CA. 2013. A liaF codon deletion abolishes daptomycin bactericidal activity against vancomycin-resistant Enterococcus faecalis. Antimicrob. Agents Chemother. 57:2831-2833. http://dx.doi.org/10.1128/AAC.00021-13.
14. Humphries RM, Kelesidis T, Tewhey R, Rose WE, Schork N, Nizet V, Sakoulas G. 2012. Genotypic and phenotypic evaluation of the evolution of high-level daptomycin nonsusceptibility in vancomycin-resistant Enterococcus faecium. Antimicrob. Agents Chemother. 56:6051-6053. http://dx.doi.org/10.1128/AAC.01318- 12.
15. Tran TT, Panesso D, Gao H, Roh JH, Munita JM, Reyes J, Diaz L, Lobos EA, Shamoo Y, Mishra NN, Bayer AS, Murray BE, Weinstock GM, Arias CA. 2013. Whole-genome analysis of a daptomycinsusceptible Enterococcus faecium strain and its daptomycin-resistant variant arising during therapy. Antimicrob. Agents Chemother. 57:261-268. http://dx.doi.org/10.1128/AAC.01454-12.
16. Munita JM, Panesso D, Diaz L, Tran TT, Reyes J, Wanger A, Murray BE, Arias CA. 2012. Correlation between mutations in liaFSR of Enterococcus faecium and MIC of daptomycin: revisiting daptomycin breakpoints. Antimicrob. Agents Chemother. 56:4354-4359. http://dx.doi.org/10.1128/AAC.00509-12.
17. Sakoulas G, Nonejuie P, Nizet V, Pogliano J, Crum-Cianflone N, Haddad F. 2013. Treatment of high-level gentamicin-resistant Enterococcus faecalis endocarditis with daptomycin plus ceftaroline. Antimicrob. Agents Chemother. 57:4042-4045. http://dx.doi.org/10.1128/AAC.02481-12.
18. Sierra-Hoffman M, Iznaola O, Goodwin M, Mohr J. 2012. Combination therapy with ampicillin and daptomycin for treatment of Enterococcus faecalis endocarditis. Antimicrob. Agents Chemother. 56:6064. http://dx.doi.org/10.1128/ AAC.01760-12.
19. Werth BJ, Sakoulas G, Rose WE, Pogliano J, Tewhey R, Rybak MJ. 2013. Ceftaroline increases membrane binding and enhances the activity of daptomycin against daptomycin-nonsusceptible vancomycinintermediate Staphylococcus aureus in a pharmacokinetic/pharmacodynamic model. Antimicrob. Agents Chemother. 57:66-73. http://dx.doi.org/10.1128/AAC.01586-12.
20. Sakoulas G, Rose W, Nonejuie P, Olson J, Pogliano J, Humphries R, Nizet V. 2014. Ceftaroline restores daptomycin activity against daptomycinnonsusceptible vancomycin-resistant Enterococcus faecium. Antimicrob. Agents Chemother. 58:1494-1500. http://dx.doi.org/10.1128/AAC.02274-13.
21. Panesso D, Reyes J, Rincón S, Díaz L, Galloway-Peña J, Zurita J, Carrillo C, Merentes A, Guzmán M, Adachi JA, Murray BE, Arias CA. 2010. Molecular epidemiology of vancomycin-resistant Enterococcus faecium: a prospective, multicenter study in South American hospitals. J. Clin. Microbiol. 48:1562-1569. http://dx.doi.org/10.1128/JCM.02526-09.
22. Clinical and Laboratory Standards Institute. 2012. MS100-S22. Performance standards for antimicrobial susceptibility testing: 21st informational supplement, vol 32. Clinical and Laboratory Standards Institute, Wayne, PA.
23. Palmer KL, Daniel A, Hardy C, Silverman J, Gilmore MS. 2011. Genetic basis for daptomycin resistance in enterococci. Antimicrob. Agents Chemother. 55:2245-2256. http://dx.doi.org/10.1128/AAC.01350-10.
24. Peleg AY, Miyakis S, Ward DV, Earl AM, Rubio A, Cameron DR, Pillai S, Moellering RCJ, Eliopoulos GM. 2012. Whole genome characterization of the mechanisms of daptomycin resistance in clinical and laboratory derived isolates of Staphylococcus aureus. PLoS One 7:e28316. http://dx.doi.org/10.1371/journal. pone.0028316.
25. Yang SJ, Mishra NN, Rubio A, Bayer AS. 2013. Causal role of single nucleotide polymorphisms within the mprF gene of Staphylococcus aureus in daptomycin resistance. Antimicrob. Agents Chemother. 57:5658-5664. http://dx.doi.org/10.1128/AAC.01184-13.
26. Bayer AS, Schneider T, Sahl HG. 2013. Mechanisms of daptomycin resistance in Staphylococcus aureus: role of the cell membrane and cell wall. Ann. N. Y. Acad. Sci. 1277:139-158. http://dx.doi.org/10.1111/j.1749-6632.2012.06819.x.
27. Yang SJ, Kreiswirth BN, Sakoulas G, Yeaman MR, Xiong YQ, Sawa A, Bayer AS. 2009. Enhanced expression of dltABCD is associated with the development of daptomycin nonsusceptibility in a clinical endocarditis isolate of Staphylococcus aureus. J. Infect. Dis. 200:1916-1920. http://dx.doi.org/10.1086/ 648473.
28. Nallapareddy SR, Weinstock GM, Murray BE. 2003. Clinical isolates of Enterococcus faecium exhibit strain-specific collagen binding mediated by Acm, a new member of the MSCRAMM family. Mol. Microbiol. 47:1733-1747. http://dx.doi.org/10.1046/j.1365-2958.2003.03417.x.
29. Qin X, Galloway-Peña JR, Sillanpaa J, Roh JH, Nallapareddy SR, Chowdhury S, Bourgogne A, Choudhury T, Muzny DM, Buhay CJ, Ding Y, Dugan-Rocha S, Liu W, Kovar C, Sodergren E, Highlander S, Petrosino JF, Worley KC, Gibbs RA, Weinstock GM, Murray BE. 2012. Complete genome sequence of Enterococcus faecium strain TX16 and comparative genomic analysis of Enterococcus faecium genomes. BMC Microbiol. 12:135. http://dx.doi.org/10.1186/1471-2180-12-135.
30. Berti AD, Sakoulas G, Nizet V, Tewhey R, Rose WE. 2013. β-Lactam antibiotics targeting PBP1 selectively enhance daptomycin activity against methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 57:5005-5012. http://dx.doi.org/10.1128/AAC.00594-13.
31. Vignaroli C, Rinaldi C, Varaldo PE. 2011. Striking "seesaw effect" between daptomycin nonsusceptibility and beta-lactam susceptibility in Staphylococcus haemolyticus. Antimicrob. Agents Chemother. 55:2495-2496. http://dx.doi.org/10.1128/AAC.00224-11.
32. Hachmann AB, Angert ER, Helmann JD. 2009. Genetic analysis of factors affecting susceptibility of Bacillus subtilis to daptomycin. Antimicrob. Agents Chemother. 53:1598-1609. http://dx.doi.org/10.1128/AAC.01329-08.
33. Hachmann AB, Sevim E, Gaballa A, Popham DL, Antelmann H, Helmann JD. 2011. Reduction in membrane phosphatidylglycerol content leads to daptomycin resistance in Bacillus subtilis. Antimicrob. Agents Chemother. 55:4326-4337. http://dx.doi.org/10.1128/AAC.01819-10.
34. Türck M, Bierbaum G. 2012. Purification and activity testing of the full-length YycFGHI proteins of Staphylococcus aureus. PLoS One 7:e30403. http://dx.doi.org/10.1371/journal.pone.0030403.
35. Szurmant H, Mohan MA, Imus PM, Hoch JA. 2007. YycH and YycI interact to regulate the essential YycFG two-component system in Bacillus subtilis. J. Bacteriol. 189:3280-3289. http://dx.doi.org/10.1128/JB.01936-06.
36. Davlieva M, Zhang W, Arias CA, Shamoo Y. 2013. Biochemical characterization of cardiolipin synthase mutations associated with daptomycin resistance in enterococci. Antimicrob. Agents Chemother. 57:289-296. http://dx.doi.org/10.1128/AAC.01743-12.
37. Friedman L, Alder JD, Silverman JA. 2006. Genetic changes that correlate with reduced susceptibility to daptomycin in Staphylococcus aureus. Antimicrob. Agents Chemother. 50:2137-2145. http://dx.doi.org/10.1128/AAC.00039-06.
38. Grogan DW, Cronan JEJ. 1997. Cyclopropane ring formation in membrane lipids of bacteria. Microbiol. Mol. Biol. Rev. 61:429-441.
39. Aravind L, Koonin EV. 1998. The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci. 23:469-472. http://dx.doi.org/10.1016/S0968-0004(98)01293-6.
40. Gustafsson C, Persson BC. 1998. Identification of the rrmA gene encoding the 23S rRNA m1G745 methyltransferase in Escherichia coli and characterization of an m1G745-deficient mutant. J. Bacteriol. 180:359-365.
41. Sakoulas G, Bayer AS, Pogliano J, Tsuji BT, Yang SJ, Mishra NN, Nizet V, Yeaman MR, Moise PA. 2012. Ampicillin enhances daptomycin- and cationic host defense peptide-mediated killing of ampicillin- and vancomycinresistant Enterococcus faecium. Antimicrob. Agents Chemother. 56:838-844. http://dx.doi.org/10.1128/AAC.05551-11.
42. Jordan S, Hutchings MI, Mascher T. 2008. Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol. Rev. 32:107-146. http://dx.doi.org/10. 1111/j.1574-6976.2007.00091.x.
43. Dubrac S, Bisicchia P, Devine KM, Msadek T. 2008. A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Mol. Microbiol. 70:1307-1322. http://dx.doi.org/10.1111/j.1365-2958. 2008.06483.x.
44. Dubrac S, Boneca IG, Poupel O, Msadek T. 2007. New insights into the WalK/WalR (YycG/YycF) essential signal transduction pathway reveal a major role in controlling cell wall metabolism and biofilm formation in Staphylococcus aureus. J. Bacteriol. 189:8257-8269. http://dx.doi.org/10.1128/JB.00645-07.
45. Mishra NN, Bayer AS, Moise PA, Yeaman MR, Sakoulas G. 2012. Reduced susceptibility to host-defense cationic peptides and daptomycin coemerge in methicillin-resistant Staphylococcus aureus from daptomycinnaive bacteremic patients. J. Infect. Dis. 206:1160-1167. http://dx.doi.org/10.1093/infdis/ jis482.
46. Mishra NN, A. Rubio, CC Nast and AS Bayer. 2012. Differential adaptations of methicillin-resistant Staphylococcus aureus to serial in vitro passage in daptomycin: evolution of daptomycin resistance and role of membrane carotenoid content and fluidity. Int. J. Microbiol. 2012:683450. http://dx.doi.org/10.1155/ 2012/683450.
47. Hancock LE, Perego M. 2004. Systematic inactivation and phenotypic characterization of two-component signal transduction systems of Enterococcus faecalis V583. J. Bacteriol. 186:7951-7958. http://dx.doi.org/10.1128/JB.186.23. 7951-7958.2004.