Staphylococcal phenotypes induced by naturally occurring and synthetic membrane-interactive polyphenolic β-lactam resistance modifiers

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Palacios, Lucia ^a   Rosado, Helena ^a   Micol, Vicente ^b   Rosato, Adriana E ^c   Bernal, Patricia ^a   Arroyo, Raquel ^a   Grounds, Helen ^a   Anderson, James C ^a   Stabler, Richard A ^d   Taylor, Peter W ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHIN GALLATE; DAPTOMYCIN; EPICATECHIN; EPICATECHIN GALLATE; EPIGALLOCATECHIN GALLATE; FLAVONOID; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT;

ANTIBIOTIC RESISTANCE; ARTICLE; ARTIFICIAL MEMBRANE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL MEMBRANE; BILAYER MEMBRANE; BINDING AFFINITY; CONTROLLED STUDY; DRUG POTENTIATION; DRUG STRUCTURE; GENE EXPRESSION; LIPID COMPOSITION; MEMBRANE BINDING; MEMBRANE FLUIDITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHARMACOPHORE; PHENOTYPE; UPREGULATION; CELL WALL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIAL SENSITIVITY TEST;

ANTI-BACTERIAL AGENTS; CELL WALL; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; PHENOTYPE;

EID: 84899106627     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093830     Document Type: Article

References (71)

1. Lazarevic V, Beaume M, Corvaglia A, Hernandez D, Schrenzel J et al. (2011) Epidemiology and virulence insights from MRSA and MSSA genome analysis. Fut Microbiol 6: 513-532.
2. Lee BY, McGlone SM, Wong KF, Yilmaz SL, Avery TR et al. (2011) Modeling the spread of methicillin-resistant Staphylococcus aureus (MRSA) outbreaks throughout the hospitals in Orange County, California. Infect Contr Hosp Epidemiol 32: 562-572.
3. Peterson LR, Hacek DM, Robicsek A (2007) 5 Million Lives Campaign. Case study: an MRSA intervention at Evanston Northwestern Healthcare. Jt Comm J Qual Patient Saf 33: 732-738.
4. Edgeworth JD (2011) Has decolonization played a central role in the decline in UK methicillin-resistant Staphylococcus aureus transmission? A focus on evidence from intensive care. J Antimicrob Chemother 66: ii41-ii47.
5. Datta R., and Huang, S S. (2008) Risk of infection and death due to methicillin-resistant Staphylococcus aureus in long-term carriers. Clin. Infect. Dis. 47, 176-181. (Pubitemid 351920617)
6. Anderson DJ, Kaye KS, Chen LF, Schmader KE, Choi Y et al. (2009) Clinical and financial outcomes due to methicillin resistant Staphylococcus aureus surgical site infection: a multi-center matched outcomes study. PLoS One 4: e8305.
7. Martinez JL, Baquero F, Andersson DI (2007) Predicting antibiotic resistance. Nat Rev Microbiol 5: 958-965. (Pubitemid 350138975)
8. Taylor PW, Bernal P, Zelmer A (2009) Modification of the bacterial phenotype as an approach to counter the emergence of multidrug-resistant pathogens. In: Bonilla AR, Muniz KP, editors. Antibiotic Resistance: Causes and Risk Factors, Mechanisms and Alternatives. Hauppauge, NY: Nova Science Publishers. pp. 43-78.
9. Cushnie TPT, Lamb AJ (2011) Recent advances in understanding the antibacterial properties of flavonoids. Int J Antimicrob Agents 38: 99-107.
10. Taylor PW, Hamilton-Miller JMT, Stapleton PD (2005) Antimicrobial properties of green tea catechins. Food Sci Technol Bull 2: 71-81.
11. Geddes AM, Klugman KP, Rolinson GN (2007) Introduction: historical perspective and development of amoxicillin/clavulanate. Int J Antimicrob Agents 30 Suppl 2: S109-112.
12. Stapleton PD, Shah S, Anderson JC, Hara Y, Hamilton-Miller JMT et al. (2004) Modulation of beta-lactam resistance in Staphylococcus aureus by catechins and gallates. Int J Antimicrob Agents 23: 462-467. (Pubitemid 38569594)
13. Taylor PW (2013) Alternative natural sources for a new generation of antibacterial agents. Int J Antimicrob Agents 42: 195-201.
14. Caturla N, Vera-Samper E, Villalain J, Reyes Mateo C, Micol V (2003) The relationship between the antioxidant and the antibacterial properties of galloylated catechins and the structure of phospholipid model membranes. Free Rad Biol Med 34: 648-662. (Pubitemid 36288531)
15. Stapleton PD, Shah S, Hara Y, Taylor PW (2006) Potentiation of catechin gallate-mediated sensitization of Staphylococcus aureus to oxacillin by nongalloylated catechins. Antimicrob Agents Chemother 50: 752-755. (Pubitemid 43190993)
16. Kajiya K, Kumazawa S, Nakayama T (2002) Effects of external factors on the interaction of tea catechins with lipid bilayers. Biosci Biotechnol Biochem 66: 2330-2335. (Pubitemid 39251166)
17. Kajiya K, Kumazawa S, Nakayama T (2001) Steric effects on interaction of tea catechins with lipid bilayers. Biosci Biotechnol Biochem 65: 2638-2643. (Pubitemid 33617851)
18. Stapleton PD, Shah S, Ehlert K, Hara Y, Taylor PW (2007) The β-lactamresistance modifier (-)-epicatechin gallate alters the architecture of the cell wall of Staphylococcus aureus. Microbiology 153: 2093-2103. (Pubitemid 47074064)
19. Bernal P, Zloh M, Taylor PW (2009) Disruption of D-alanyl esterification of Staphylococcus aureus cell wall teichoic acid by the b-lactam resistance modifier (-)- epicatechin gallate. J Antimicrob Chemother 63: 1156-1162.
20. Stapleton PD, Gettert J, Taylor PW (2006) Epicatechin gallate, a component of green tea, reduces halotolerance in Staphylococcus aureus. Int J Food Microbiol 111: 276-279. (Pubitemid 44374085)
21. Chambers HF, DeLeo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7: 629-641.
22. Pinho MG, de Lencastre H, Tomasz A (2001) An acquired and a native penicillin-binding protein cooperate in building the cell wall of drug-resistant staphylococci. Proc Natl Acad Sci USA 98: 10886-10891. (Pubitemid 32878714)
23. Pinho MG, Errington J (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Molec Microbiol 50: 871-881. (Pubitemid 37372250)
24. Turner RD, Ratcliffe EC, Wheeler R, Golestanian R, Hobbs JK et al. (2010) Peptidoglycan architecture can specify division planes in Staphylococcus aureus. Nat Commun 1:26. doi:10.1038/ncomms1025.
25. Pinho MG, Errington J (2005) Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Molec Microbiol 55: 799-807. (Pubitemid 40203695)
26. Bernal P, Lemaire S, Pinho MG, Mobashery S, Hinds J et al. (2010) Insertion of epicatechin gallate into the cytoplasmic membrane of methicillin-resistant Staphylococcus aureus disrupts penicillin-binding protein (PBP) 2a-mediated β-lactam resistance by delocalizing PBP2. J Biol Chem 285: 24055-24065.
27. Short SA, White DC (1971) Metabolism of phosphatidylglycerol, lysylphosphatidylglycerol, and cardiolipin of Staphylococcus aureus. J Bacteriol 108: 219-226.
28. Mukhopadhyay K, Whitmire W, Xiong YQ, Molden J, Jones T et al. (2007) In vitro susceptibility of Staphylococcus aureus to thrombin-induced platelet microbicidal protein-1 (tPMP-1) is influenced by cell membrane phospholipid composition and asymmetry. Microbiology 153: 1187-1197. (Pubitemid 46605817)
29. Wilkinson BJ, Muthaiyan A, Jayaswal K (2005) The cell wall stress stimulon of Staphylococcus aureus and other gram-positive bacteria. Curr Med Chem -Anti-Infect Agents 4: 259-276.
30. Muthaiyan A, Silverman JA, Jayaswal RK, Wilkinson BJ (2008) Transcriptional profiling reveals that daptomycin induces the Staphylococcus aureus cell wall stress stimulon and genes responsive to membrane depolarization. Antimicrob Agents Chemother 52: 980-990. (Pubitemid 351358377)
31. Tsuchiya H (2001) Stereospecificity in membrane effects of catechins. Chem-Biol Interact 134: 41-54.
32. Anderson JC, Headley C, Stapleton PD, Taylor PW (2005) Asymmetric total synthesis of B-ring modified (-)-epicatechin gallate analogues and their modulation of β-lactam resistance in Staphylococcus aureus. Tetrahedron 61: 7703-7711. (Pubitemid 40957007)
33. Anderson JC, McCarthy RM, Paulin S, Taylor PW (2011) Synthesis and antibacterial activity of hydrolytically stable (-)-epicatechin gallate analogues for the modulation of β-lactam resistance in Staphylococcus aureus. Bioorg Med Chem Lett 21: 6996-7000.
34. Mehta S, Singh C, Plata KB, Chanda PK, Paul A et al. (2012) β-lactams increase the antibacterial activity of daptomycin against clinical methicillin-resistant Staphylococcus aureus strains and prevent selection of daptomycin-resistant derivatives. Antimicrob Agents Chemother 56: 6192-6200.
35. Inoue R, Kaito C, Tanabe M, Kamura K, Akimitsu N et al., (2001) Genetic identification of two distinct DNA polymerases, DnaE and PolC, that are essential for chromosomal DNA replication in Staphylococcus aureus. Mol Genet Genom 266: 564-571. (Pubitemid 33145118)
36. Ichihashi N, Kurokawa K, Matsuo M, Kaito C, Sekimizu K (2003) Inhibitory effects of basic or neutral phospholipid on acidic phospholipid-mediated dissociation of adenine nucleotide bound to DnaA protein, the initiator of chromosomal DNA replication. J Biol Chem 278: 28778-28786. (Pubitemid 36935787)
37. Mehta S, Cuirolo AX, Plata KB, Riosa S, Silverman JA et al. (2012) VraSR two-component regulatory system contributes to mprF-mediated decreased susceptibility to daptomycin in in vivo-selected clinical strains of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 56: 92-102.
38. Bernal P, Munoz-Rojas J, Hurtado A, Ramos JL, Segura A (2007) A Pseudomonas putida cardiolipin synthesis mutant exhibits increased sensitivity to drugs related to transport functionality. Environ Microbiol 9: 1135-1145. (Pubitemid 46697270)
39. Witney AA, Marsden GL, Holden MT, Stabler RA, Husain SE et al. (2005) Design, validation, and application of a seven-strain Staphylococcus aureus PCR product microarray for comparative genomics. Appl Environ Microbiol 71: 7504-7514. (Pubitemid 43194244)
40. Doyle M, Feuerbaum EA, Fox KR, Hinds J, Thurston DE et al. (2009) Response of Staphylococcus aureus to subinhibitory concentrations of a sequence-selective, DNA minor groove cross-linking pyrrolobenzodiazepine dimer. J Antimicrob Chemother 64: 949-959.
41. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: 1-25.
42. Smyth GK, Michaud J, Scott HS (2005) Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 21: 2067-2075. (Pubitemid 40668046)
43. Funes L, Laporta O, Cerdan-Calero M, Micol V (2010) Effects of verbascoside, a phenylpropanoid glycoside from lemon verbena, on phospholipid model membranes. Chem Phys Lipids 163: 190-199.
44. Wardlaw JR, Sawyer WH, Ghiggino KP (1987) Vertical fluctuations of phospholipid acyl chains in bilayers. FEBS Lett 223: 20-24.
45. Eftink MR, Ghiron CA (1976) Fluorescence quenching of indole and model micelle systems. J Phys Chem 80: 486-493.
46. Laporta O, Pérez-Fons L, Mallavia R, Caturla N, Micol V (2007) Isolation, characterization and antioxidant capacity assessment of the bioactive compounds derived from Hypoxis rooperi corm extract (African potato) Food Chem 101: 1425-1437. (Pubitemid 44488570)
47. Dengler V, Meier PS, Heusser R, Berger-Bächi B, McCallum N (2011) Induction kinetics of the Staphylococcus aureus cell wall stress stimulon in response to different cell wall active antibiotics. BMC Microbiol 11: 16.
48. Utaida S, Dunman PM, Macapagal D, Murphy E, Projan SJ et al (2003) Genome-wide transcriptional profiling of the response of Staphylococcus aureus to cell-wall-active antibiotics reveals a cell-wall-stress stimulon. Microbiology 149: 2719-2732. (Pubitemid 37279247)
49. McAleese F, Wu SW, Sieradski K, Dunman P, Murphy E et al. (2006) Overexpression of genes of the cell wall stimulon in clinical isolates of Staphylococcus aureus exhibiting vancomycin-intermediate-S. aureus-type resistance to vancomycin. J Bacteriol 188: 1120-1133. (Pubitemid 43146428)
50. Boyle-Vavra S, Yin S, Jo DS, Montgomery CP, Daum RS (2013) VraT/YvqF is required for methicillin resistance and activation of the VraSR regulon in Staphylococcus aureus. Antimicrob Agents Chemother 57: 83-95.
51. Jousselin A, Renzoni A, Andrey DO, Monod A, Lew DP et al. (2012) The posttranslocational chaperone lipoprotein PrsA is involved in both glycopeptide and oxacillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 56: 3629-3640.
52. Hübscher J, McCallum N, Sifri CD, Majcherczyk PA, Entenza JM et al. (2009) MsrR contributes to cell surface characteristics and virulence in Staphylococcus aureus. FEMS Microbiol Lett 295: 251-60.
53. Stapleton MR, Horsburgh MJ, Hayhurst EJ, Wright L, Jonsson IM et al. (2007) Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J Bacteriol 189: 7316-7325. (Pubitemid 47557346)
54. Shah S, Stapleton PD, Taylor PW (2008) The polyphenol (-)-epicatechin gallate disrupts the secretion of virulence-related proteins by Staphylococcus aureus. Lett Appl Microbiol 46: 181-185.
55. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Molec Microbiol 48: 1429-1449.
56. Falord M, Mäder U, Hiron A, Débarbouillé M, Msadek T (2011) Investigation of the Staphylococcus aureus GraSR regulon reveals novel links to virulence, stress response and cell wall signal transduction pathways. PLoS One 6: e21323.
57. Peschel A, Jack RW, Otto M, Collins LV, Staubitz P et al. (2001) Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with Llysine. J Exp Med 193: 1067-1076. (Pubitemid 32436200)
58. Andrä J, Goldmann T, Ernst CM, Peschel A, Gutsmann T (2011) Multiple peptide resistance factor (MprF)-mediated Resistance of Staphylococcus aureus against antimicrobial peptides coincides with a modulated peptide interaction with artificial membranes comprising lysyl-phosphatidylglycerol. J Biol Chem 286: 18692-18700.
59. Mishra NN, Yang SJ, Sawa A, Rubio A, Nast CC et al. (2009) Analysis of cell membrane characteristics of in vitro-selected daptomycin-resistant strains of methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 53: 2312-2318.
60. Trevors JT (2003) Fluorescent probes for bacterial cytoplasmic membrane research. J Biochem Biophys Meth 57: 87-103.
61. Sirk TW, Brown EF, Sum AK, Friedman M (2008) Molecular dynamics study on the biophysical interactions of seven green tea catechins with lipid bilayers of cell membranes. J Agric Food Chem 56: 7750-7758.
62. Kajiya K, Kumazawa S, Naito A, Nakayama T (2008) Solid-state NMR analysis of the orientation and dynamics of epigallocatechin gallate, a green tea polyphenol, incorporated into lipid bilayers. Magn Reson Chem 46: 174-177.
63. Trotter PJ, Storch J (1989) 3-[ p-(6-phenyl)-1,3,5-hexatrienyl] phenylpropionic acid (PA-DPH): characterization as a fluorescent membrane probe and binding to fatty acid binding proteins. Biochim Biophys Acta 982: 131-139. (Pubitemid 19159058)
64. Kaiser RD, London E (1998) Location of diphenylhexatriene (DPH) and its derivatives within membranes: comparison of different fluorescence quenching analyses of membrane depth. Biochemistry 37: 8180-8190. (Pubitemid 28307081)
65. Davenport L, Dale RE, Bisby RH, Cundall RB (1985) Transverse location of the fluorescent probe 1,6-diphenyl-1,3,5-hexatriene in model lipid bilayer membrane systems by resonance excitation energy transfer. Biochemistry 24: 4097-4108.
66. Pérez-Fons L, Garzón MT, Micol V (2010) Relationship between the antioxidant capacity and effect of rosemary (Rosmarinus officinalis L.) polyphenols on membrane phospholipid order. J Agric Food Chem 58: 161-171.
67. Ernst CM, Staubitz P, Mishra NN, Yang SJ, Hornig G et al. (2009) The bacterial defensin resistance protein MprF consists of separable domains for lipid lysinylation and antimicrobial peptide repulsion. PLoS Pathog 5: e1000660.
68. Bertsche U, Weidenmaier C, Kuehner D, Yang SJ, Baur S et al. (2011) Correlation of daptomycin resistance in a clinical Staphylococcus aureus strain with increased cell wall teichoic acid production and D-alanylation. Antimicrob Agents Chemother 55: 3922-2928.
69. Sass P, Bierbaum G (2009) Native graS mutation supports the susceptibility of Staphylococcus aureus strain SG511 to antimicrobial peptides. Int J Med Microbiol 299: 313-322.
70. López D, Kolter R (2010) Functional microdomains in bacterial membranes. Genes Dev 24: 1893-1902.
71. Rosado H, O'Neill AJ, Blake KL, Walther M, Long PF et al. (2012) Rotating wall vessel exposure alters protein secretion and global gene expression in Staphylococcus aureus. Int J Astrobiol 11: 71-81.