Exposure of Clinical MRSA Heterogeneous Strains to β-Lactams Redirects Metabolism to Optimize Energy Production through the TCA Cycle

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Keaton, Mignon A ^b   Rosato, Roberto R ^a   Plata, Konrad B ^a   Singh, Christopher R ^a   Rosato, Adriana E ^a  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b METABOLON INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; BETA LACTAM ANTIBIOTIC; CITRIC ACID; OXACILLIN; TRICARBOXYL CITRIC ACID; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; AMINO ACID TRANSPORT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL STRAIN; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CATABOLISM; CELL FUNCTION; CELL SURVIVAL; CIS ACONITASE GENE; CONTROLLED STUDY; DNA DAMAGE; ENERGY METABOLISM; ENERGY YIELD; GENE EXPRESSION; GENE INACTIVATION; LIQUID CHROMATOGRAPHY; MASS FRAGMENTOGRAPHY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 84881098200     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071025     Document Type: Article

References (40)

1. Herold BC, Immergluck LC, Maranan MC, Lauderdale DS, Gaskin RE, et al. (1998) Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA 279: 593-598.
2. Georgopapadakou NH, (1993) Penicillin-binding proteins and bacterial resistance to beta-lactams. Antimicrob Agents Chemother 37: 2045-2053.
3. Finan JE, Rosato AE, Dickinson TM, Ko D, Archer GL, (2002) Conversion of oxacillin-resistant staphylococci from heterotypic to homotypic resistance expression. Antimicrob Agents Chemother 46: 24-30.
4. Forbes BA, Bombicino K, Plata K, Cuirolo A, Webber D, et al. (2008) Unusual form of oxacillin resistance in methicillin-resistant Staphylococcus aureus clinical strains. Diagn Microbiol Infect Dis 61: 387-395.
5. Cuirolo A, Plata K, Rosato AE, (2009) Development of homogeneous expression of resistance in methicillin-resistant Staphylococcus aureus clinical strains is functionally associated with a beta-lactam-mediated SOS response. J Antimicrob Chemother 64: 37-45.
6. Tomasz A, Nachman S, Leaf H, (1991) Stable classes of phenotypic expression in methicillin-resistant clinical isolates of staphylococci. Antimicrob Agents Chemother 35: 124-129.
7. Seidl K, Muller S, Francois P, Kriebitzsch C, Schrenzel J, et al. (2009) Effect of a glucose impulse on the CcpA regulon in Staphylococcus aureus. BMC Microbiol 9: 95.
8. Nelson JL, Rice KC, Slater SR, Fox PM, Archer GL, et al. (2007) Vancomycin-intermediate Staphylococcus aureus strains have impaired acetate catabolism: implications for polysaccharide intercellular adhesin synthesis and autolysis. Antimicrob Agents Chemother 51: 616-622.
9. Somerville GA, Chaussee MS, Morgan CI, Fitzgerald JR, Dorward DW, et al. (2002) Staphylococcus aureus aconitase inactivation unexpectedly inhibits post-exponential-phase growth and enhances stationary-phase survival. Infect Immun 70: 6373-6382.
10. Krebs HA, (1937) Dismutation of pyruvic acid in Gonococcus and Staphylococcus. Biochem J 31: 661-671.
11. Collins FM, Lascelles J, (1962) The effect of growth conditions on oxidative and dehydrogenase activity in Staphylococcus aureus. J Gen Microbiol 29: 531-535.
12. Kriegeskorte A, Konig S, Sander G, Pirkl A, Mahabir E, et al. (2011) Small colony variants of Staphylococcus aureus reveal distinct protein profiles. Proteomics 11: 2476-2490.
13. Goldstein F, Perutka J, Cuirolo A, Plata K, Faccone D, et al. (2007) Identification and phenotypic characterization of a beta-lactam-dependent, methicillin-resistant Staphylococcus aureus strain. Antimicrob Agents Chemother 51: 2514-2522.
14. Plata KB, Rosato RR, Rosato AE, (2011) Fate of mutation rate depends on agr locus expression during oxacillin-mediated heterogeneous-homogeneous selection in methicillin-resistant Staphylococcus aureus clinical strains. Antimicrob Agents Chemother 55: 3176-3186.
15. Kim MS, Shin J, Lee W, Lee HS, Oh BH, (2003) Crystal structures of RbsD leading to the identification of cytoplasmic sugar-binding proteins with a novel folding architecture. J Biol Chem 278: 28173-28180.
16. Deutscher J, Francke C, Postma PW, (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70: 939-1031.
17. Scheffers DJ, Pinho MG, (2005) Bacterial cell wall synthesis: new insights from localization studies. Microbiol Mol Biol Rev 69: 585-607.
18. Yasbin RE, (1977) DNA repair in Bacillus subtilis. II. Activation of the inducible system in competent bacteria. Mol Gen Genet 153: 219-225.
19. Bizzini A, Entenza JM, Moreillon P, (2007) Loss of penicillin tolerance by inactivating the carbon catabolite repression determinant CcpA in Streptococcus gordonii. J Antimicrob Chemother 59: 607-615.
20. Starai VJ, Escalante-Semerena JC, (2004) Acetyl-coenzyme A synthetase (AMP forming). Cell Mol Life Sci 61: 2020-2030.
21. Weissenborn DL, Wittekindt N, Larson TJ, (1992) Structure and regulation of the glpFK operon encoding glycerol diffusion facilitator and glycerol kinase of Escherichia coli K-12. J Biol Chem 267: 6122-6131.
22. Pinho MG, Errington J, (2005) Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Mol Microbiol 55: 799-807.
23. Berger-Bachi B, Rohrer S, (2002) Factors influencing methicillin resistance in staphylococci. Arch Microbiol 178: 165-171.
24. Formstone A, Carballido-Lopez R, Noirot P, Errington J, Scheffers DJ, (2008) Localization and interactions of teichoic acid synthetic enzymes in Bacillus subtilis. J Bacteriol 190: 1812-1821.
25. Swenson JM, Lonsway D, McAllister S, Thompson A, Jevitt L, et al. (2007) Detection of mecA-mediated resistance using reference and commercial testing methods in a collection of Staphylococcus aureus expressing borderline oxacillin MICs. Diagn Microbiol Infect Dis 58: 33-9.
26. Gardner JF, Lascelles J, (1962) The requirement for acetate of a streptomycin-resistant strain of Staphylococcus aureus. J Gen Microbiol 29: 157-164.
27. Goldschmidt MC, Powelson DM, (1953) Effect of the culture medium on the oxidation of acetate by Micrococcus pyogenes var. aureus. Arch Biochem Biophys 46: 154-163.
28. Massilamany C, Gangaplara A, Gardner DJ, Musser JM, Steffen D, et al. (2011) TCA cycle inactivation in Staphylococcus aureus alters nitric oxide production in RAW 264.7 cells. Mol Cell Biochem 355: 75-82.
29. Friedman DB, Stauff DL, Pishchany G, Whitwell CW, Torres VJ, et al. (2006) Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2: e87.
30. Birkenstock T, Liebeke M, Winstel V, Krismer B, Gekeler C, et al. (2012) Exometabolome analysis identifies pyruvate dehydrogenase as a target for the antibiotic triphenylbismuthdichloride in multiresistant bacterial pathogens. J Biol Chem 287: 2887-2895.
31. Sadykov MR, Mattes TA, Luong TT, Zhu Y, Day SR, et al. (2010) Tricarboxylic acid cycle-dependent synthesis of Staphylococcus aureus Type 5 and 8 capsular polysaccharides. J Bacteriol 192: 1459-1462.
32. Novick R, (1967) Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. Virology 33: 155-166.
33. Sreekumar A, Poisson LM, Rajendiran TM, Khan AP, Cao Q, et al. (2009) Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 457: 910-914.
34. Boudonck KJ, Mitchell MW, Nemet L, Keresztes L, Nyska A, et al. (2009) Discovery of metabolomics biomarkers for early detection of nephrotoxicity. Toxicol Pathol 37: 280-292.
35. Lawton KA, Berger A, Mitchell M, Milgram KE, Evans AM, et al. (2008) Analysis of the adult human plasma metabolome. Pharmacogenomics 9: 383-397.
36. Evans AM, Dehaven CD, Barrett T, Mitchell M, Milgram E, (2009) Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems. Anal Chem 81: 6656-6667.
37. Dehaven CD, Evans AM, Dai H, Lawton KA, (2010) Organization of GC/MS and LC/MS metabolomics data into chemical libraries. J Cheminform 2 9: 1758-2946.
38. Storey JD, Tibshirani R, (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445.
39. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
40. McKinney TK, Sharma VK, Craig WA, Archer GL, (2001) Transcription of the gene mediating methicillin resistance in Staphylococcus aureus (mecA) is corepressed but not coinduced by cognate mecA and beta-lactamase regulators. J Bacteriol 183: 6862-6868.