Biochemical characterization of cardiolipin synthase mutations associated with daptomycin resistance in enterococci

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 1, 2013, Pages 289-296

  Davlieva, Milya ^a   Zhang, Wanna ^a   Arias, Cesar A ^b,c   Shamoo, Yousif ^a  

^a RICE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSIDAD EL BOSQUE   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL ENZYME; CARDIOLIPIN; CARDIOLIPIN SYNTHASE; DAPTOMYCIN; PHOSPHATIDYLGLYCEROL; PHOSPHOLIPASE D; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; CELL MEMBRANE; ENTEROCOCCUS FAECIUM; ENZYME ACTIVITY; GENE MUTATION; GENETIC VARIABILITY; NONHUMAN; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; STREPTOMYCES;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CARDIOLIPINS; CATALYTIC DOMAIN; DAPTOMYCIN; DRUG RESISTANCE, BACTERIAL; ENTEROCOCCUS FAECALIS; ENTEROCOCCUS FAECIUM; EPISTASIS, GENETIC; ESCHERICHIA COLI; KINETICS; LIPID METABOLISM; MEMBRANE PROTEINS; MODELS, MOLECULAR; MUTATION; PHOSPHATIDYLGLYCEROLS; PHOSPHOLIPASE D; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; STREPTOMYCES; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

EID: 84872013455     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01743-12     Document Type: Article

References (46)

1. Arias CA, Murray BE. 2012. The rise of the Enterococcus: beyond vancomycin resistance. Nat. Rev. Microbiol. 10:266-278.
2. Storm JC, Diekema DJ, Kroeger JS, Johnson SJ, Johannsson B. 2012. Daptomycin exposure precedes infection and/or colonization with daptomycin non-susceptible enterococcus. Antimicrob. Resist. Infect. Control 1:19.
3. Rice LB. 2008. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J. Infect. Dis. 197:1079-1081.
4. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. 2009. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis. 48:1-12.
5. Baltz RH, Miao V, Wrigley SK. 2005. Natural products to drugs: daptomycin and related lipopeptide antibiotics. Nat. Prod. Rep. 22:717-741.
6. Fowler VG, Jr, Boucher HW, Corey GR, Abrutyn E, Karchmer AW, Rupp ME, Levine DP, Chambers HF, Tally FP, Vigliani GA, Cabell CH, Link AS, DeMeyer I, Filler SG, Zervos M, Cook P, Parsonnet J, Bernstein JM, Price CS, Forrest GN, Fatkenheuer G, Gareca M, Rehm SJ, Brodt HR, Tice A, Cosgrove SE. 2006. Daptomycin versus standard therapy for bacteremia and endocarditis caused by Staphylococcus aureus. N. Engl. J. Med. 355:653-665.
7. Eliopoulos GM, Willey S, Reiszner E, Spitzer PG, Caputo G, Moellering RC, Jr. 1986. In vitro and in vivo activity of LY 146032, a new cyclic lipopeptide antibiotic. Antimicrob. Agents Chemother. 30:532-535.
8. Fass RJ, Helsel VL. 1986. In vitro activity of LY146032 against staphylococci, streptococci, and enterococci. Antimicrob. Agents Chemother. 30: 781-784.
9. Jones RN, Barry AL. 1987. Antimicrobial activity and spectrum of LY146032, a lipopeptide antibiotic, including susceptibility testing recommendations. Antimicrob. Agents Chemother. 31:625-629.
10. Tally FP, DeBruin MF. 2000. Development of daptomycin for gram-positive infections. J. Antimicrob. Chemother. 46:523-526.
11. Tally FP, Zeckel M, Wasilewski MM, Carini C, Berman CL, Drusano GL, Oleson FB, Jr. 1999. Daptomycin: a novel agent for Gram-positive infections. Expert. Opin. Investig. Drugs 8:1223-1238.
12. Sader HS, Moet GJ, Farrell DJ, Jones RN. 2011. Antimicrobial susceptibility of daptomycin and comparator agents tested against methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci: trend analysis of a 6-year period in US medical centers (2005-2010). Diagn. Microbiol. Infect. Dis. 70:412-416.
13. Hayden MK, Rezai K, Hayes RA, Lolans K, Quinn JP, Weinstein RA. 2005. Development of daptomycin resistance in vivo in methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 43:5285-5287.
14. Marty FM, Yeh WW, Wennersten CB, Venkataraman L, Albano E, Alyea EP, Gold HS, Baden LR, Pillai SK. 2006. Emergence of a clinical daptomycin-resistant Staphylococcus aureus isolate during treatment of methicillin-resistant Staphylococcus aureus bacteremia and osteomyelitis. J. Clin. Microbiol. 44:595-597.
15. Peleg AY, Miyakis S, Ward DV, Earl AM, Rubio A, Cameron DR, Pillai S, Moellering RC, Jr, 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. doi: 10.1371/journal.pone.0028316.
16. Skiest DJ. 2006. Treatment failure resulting from resistance of Staphylococcus aureus to daptomycin. J. Clin. Microbiol. 44:655-656.
17. Green MR, Anasetti C, Sandin RL, Rolfe NE, Greene JN. 2006. Development of daptomycin resistance in a bone marrow transplant patient with vancomycin-resistant Enterococcus durans. J. Oncol. Pharm. Pract. 12:179-181.
18. 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. 49:1664-1665.
19. 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.
20. Palmer KL, Daniel A, Hardy C, Silverman J, Gilmore MS. 2011. Genetic basis for daptomycin resistance in enterococci. Antimicrob. Agents Chemother. 55:3345-3356.
21. 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.
22. Silverman JA, Perlmutter NG, Shapiro HM. 2003. Correlation of daptomycin bactericidal activity and membrane depolarization in Staphylococcus aureus. Antimicrob. Agents Chemother. 47:2538-2544.
23. Pogliano J, Pogliano N, Silverman J. 2012. Daptomycin-mediated reorganization of membrane architecture causes mislocalization of essential cell division proteins. J. Bacteriol. 194:4494-4504.
24. 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.
25. 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 non-susceptibility in vancomycin-resistant Enterococcus faecium. Antimicrob. Agents Chemother. 56:6051-6053.
26. Tran TT, Panesso D, Gao H, Roh JH, Munita JM, Reyes J, Diaz L, Lobos E, Mishra NN, Bayer AS, Murray BE, Weinstock GM, Arias CA. 2012. Whole-genome analysis of daptomycin-susceptible Enterococcus faecium and its resistant derivative that arose during therapy. Antimicrob. Agents Chemother. [Epub ahead of print.] doi:10.1128/AAC.01454-12.
27. Snider C, Jayasinghe S, Hristova K, White SH. 2009. MPEx: a tool for exploring membrane proteins. Protein Sci. 18:2624-2628.
28. Uesugi Y, Hatanaka T. 2009. Phospholipase D mechanism using Streptomyces PLD. Biochim. Biophys. Acta 1791:962-969.
29. Leiros I, McSweeney S, Hough E. 2004. The reaction mechanism of phospholipase D from Streptomyces sp. strain PMF. Snapshots along the reaction pathway reveal a pentacoordinate reaction intermediate and an unexpected final product. J. Mol. Biol. 339:805-820.
30. Stuckey JA, Dixon JE. 1999. Crystal structure of a phospholipase D family member. Nat. Struct. Biol. 6:278-284.
31. Mishra NN, Bayer AS, Tran TT, Shamoo Y, Mileykovskaya E, Dowhan W, Guan Z, Arias CA. 2012. Daptomycin resistance in enterococci is associated with distinct alterations of cell membrane phospholipid content. PLoS One 7:e43958. doi:10.1371/journal.pone.0043958.
32. Hiraoka S, Nukui K, Uetake N, Ohta A, Shibuya I. 1991. Amplification and substantial purification of cardiolipin synthase of Escherichia coli. J. Biochem. 110:443-449.
33. Morii H, Goldfine H. 1991. Phosphatidyltransferase activity in Bacillus megaterium. J. Gen. Microbiol. 137:1635-1639.
34. Short SA, White DC. 1972. Biosynthesis of cardiolipin from phosphatidylglycerol in Staphylococcus aureus. J. Bacteriol. 109:820-826.
35. Tunaitis E, Cronan JE, Jr. 1973. Characterization of the cardiolipin synthetase activity of Escherichia coli envelopes. Arch. Biochem. Biophys. 155:420-427.
36. Eshaghi S, Hedren M, Nasser MI, Hammarberg T, Thornell A, Nordlund P. 2005. An efficient strategy for high-throughput expression screening of recombinant integral membrane proteins. Protein Sci. 14:676-683.
37. Prive GG. 2007. Detergents for the stabilization and crystallization of membrane proteins. Methods 41:388-397.
38. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675.
39. Perez-Iratxeta C, Andrade-Navarro MA. 2008. K2D2: estimation of protein secondary structure from circular dichroism spectra. BMC Struct. Biol. 8:25. doi:10.1186/1472-6807-8-25.
40. Kuchler K, Dohlman HG, Thorner J. 1993. The a-factor transporter (STE6 gene product) and cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 120:1203-1215.
41. O'Malley MA, Mancini JD, Young CL, McCusker EC, Raden D, Robinson AS. 2009. Progress toward heterologous expression of active G-protein-coupled receptors in Saccharomyces cerevisiae: linking cellular stress response with translocation and trafficking. Protein Sci. 18:2356-2370.
42. Greenfield NJ. 2006. Using circular dichroism spectra to estimate protein secondary structure. Nat. Protoc. 1:2876-2890.
43. Venyaminov SY, Baikalov IA, Shen ZM, Wu CS, Yang JT. 1993. Circular dichroic analysis of denatured proteins: inclusion of denatured proteins in the reference set. Anal. Biochem. 214:17-24.
44. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.
45. Zhang Y, Skolnick J. 2005. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res. 33:2302-2309.
46. Mileykovskaya E, Dowhan W. 2009. Cardiolipin membrane domains in prokaryotes and eukaryotes. Biochim. Biophys. Acta 1788:2084-2091.