Thiazolidione derivatives targeting the histidine kinase YycG are effective against both planktonic and biofilm-associated Staphylococcus epidermidis

Acta Pharmacologica Sinica

Volumn 33, Issue 3, 2012, Pages 418-425

  Huang, Ren Zheng ^a,c   Zheng, Li Kang ^b   Liu, Hua Yong ^a   Pan, Bin ^b   Hu, Jian ^a   Zhu, Tao ^a   Wang, Wei ^a   Jiang, Dan Bin ^c   Wu, Yang ^a   Wu, You Cong ^a   Han, Shi Qing ^b   Qu, Di ^a  

^a FUDAN UNIVERSITY   (China)

^b NANJING TECH UNIVERSITY   (China)

^c MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

antibacterial agent; biofilm killing activity; half maximal inhibitory concentration; minimal inhibitory concentration; Staphylococcus epidermidis

Indexed keywords

H2 10; H2 12; H2 20; H2 27; H2 28; H2 29; PROTEIN HISTIDINE KINASE; THIAZOLIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACTERICIDAL ACTIVITY; BIOFILM; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENCY; ERYTHROCYTE; HEMOLYSIS; HUMAN; HUMAN CELL; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; STAPHYLOCOCCUS EPIDERMIDIS; VERO CELL;

ANTI-BACTERIAL AGENTS; BIOFILMS; PLANKTON; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS EPIDERMIDIS; THIAZOLES;

EID: 84863235693     PISSN: 16714083     EISSN: 17457254     Source Type: Journal    
DOI: 10.1038/aps.2011.166     Document Type: Article

References (53)

1. Rupp ME, Archer GL. Coagulase-negative staphylococci: pathogens associated with medical progress. Clin Infect Dis 1994; 19: 231-43; quiz 44-5.
2. Huebner J, Goldmann DA. Coagulase-negative staphylococci: role as pathogens. Annu Rev Med 1999; 50: 223-36. (Pubitemid 29117063)
3. Mermel LA, Farr BM, Sherertz RJ, Raad II, O'Grady N, Harris JS, et al. Guidelines for the management of intravascular catheter-related infections. Infect Control Hosp Epidemiol 2001; 22: 222-42. (Pubitemid 32448672)
4. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-93. (Pubitemid 34303762)
5. Vandecasteele SJ, Peetermans WE, Merckx R, Van Eldere J. Expression of biofilm-associated genes in Staphylococcus epidermidis during in vitro and in vivo foreign body infections. J Infect Dis 2003; 188: 730-7. (Pubitemid 37115186)
6. Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005; 436: 1171-5. (Pubitemid 41232296)
7. Raad I, Alrahwan A, Rolston K. Staphylococcus epidermidis: emerging resistance and need for alternative agents. Clin Infect Dis 1998; 26: 1182-7. (Pubitemid 28215486)
8. Zhang YQ, Ren SX, Li HL, Wang YX, Fu G, Yang J, et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 2003; 49: 1577-93. (Pubitemid 37153517)
9. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, Ravel J, et al. Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 2005; 187: 2426-38. (Pubitemid 40389140)
10. Stock AM, Wylie DC, Mottonen JM, Lupas AN, Ninfa EG, Ninfa AJ, et al. Phosphoproteins involved in bacterial signal transduction. Cold Spring Harb Symp Quant Biol 1988; 53: 49-57. (Pubitemid 20007835)
11. Stock AM, Robinson VL, Goudreau PN. Two-component signal transduction. Annu Rev Biochem 2000; 69: 183-215.
12. West AH, Stock AM. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 2001; 26: 369-76. (Pubitemid 32530655)
13. Barrett JF, Hoch JA. Two-component signal transduction as a target for microbial anti-infective therapy. Antimicrob Agents Chemother 1998; 42: 1529-36. (Pubitemid 28311536)
14. Stephenson K, Hoch JA. Two-component and phosphorelay signaltransduction systems as therapeutic targets. Curr Opin Pharmacol 2002; 2: 507-12.
15. Stephenson K, Hoch JA. Virulence-and antibiotic resistanceassociated two-component signal transduction systems of Grampositive pathogenic bacteria as targets for antimicrobial therapy. Pharmacol Ther 2002; 93: 293-305. (Pubitemid 34615570)
16. Fabret C, Hoch JA. A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J Bacteriol 1998; 180: 6375-83. (Pubitemid 28544271)
17. Fukuchi K, Kasahara Y, Asai K, Kobayashi K, Moriya S, Ogasawara N. The essential two-component regulatory system encoded by yycF and yycG modulates expression of the ftsAZ operon in Bacillus subtilis. Microbiology 2000; 146: 1573-83. (Pubitemid 30458712)
18. Martin PK, Li T, Sun D, Biek DP, Schmid MB. Role in cell permeability of an essential two-component system in Staphylococcus aureus. J Bacteriol 1999; 181: 3666-73. (Pubitemid 29283792)
19. Dubrac S, Boneca IG, Poupel O, Msadek T. 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 2007; 189: 8257-69. (Pubitemid 350178938)
20. Dubrac S, Msadek T. Tearing down the wall: peptidoglycan metabolism and the WalK/WalR (YycG/YycF) essential two-component system. Adv Exp Med Biol 2008; 631: 214-28.
21. Okada A, Igarashi M, Okajima T, Kinoshita N, Umekita M, Sawa R, et al. Walkmycin B targets WalK (YycG), a histidine kinase essential for bacterial cell growth. J Antibiot (Tokyo) 2010; 63: 89-94.
22. Watanabe T, Hashimoto Y, Yamamoto K, Hirao K, Ishihama A, Hino M, et al. Isolation and characterization of inhibitors of the essential histidine kinase, YycG in Bacillus subtilis and Staphylococcus aureus. J Antibiot (Tokyo) 2003; 56: 1045-52. (Pubitemid 38128966)
23. Yamamoto K, Kitayama T, Minagawa S, Watanabe T, Sawada S, Okamoto T, et al. Antibacterial agents that inhibit histidine protein kinase YycG of Bacillus subtilis. Biosci Biotechnol Biochem 2001; 65: 2306-10. (Pubitemid 33617208)
24. Qin Z, Zhang J, Xu B, Chen L, Wu Y, Yang X, et al. Structure-based discovery of inhibitors of the YycG histidine kinase: new chemical leads to combat Staphylococcus epidermidis infections. BMC Microbiol 2006; 6: 96.
25. Qin Z, Lee B, Yang L, Zhang J, Yang X, Qu D, et al. Antimicrobial activities of YycG histidine kinase inhibitors against Staphylococcus epidermidis biofilms. FEMS Microbiol Lett 2007; 273: 149-56. (Pubitemid 47084005)
26. Pan B, Huang RZ, Han SQ, Qu D, Zhu ML, Wei P, et al. Design, synthesis, and antibiofilm activity of 2-arylimino-3-aryl-thiazolidine-4-ones. Bioorg Med Chem Lett 2010; 20: 2461-4.
27. Clinical and Laboratory Standards Institute: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 7th ed. In Approved standard M7-A7 Clinical and Laboratory Standards Institute, Villanova, PA, USA; 2006.
28. Christensen GD, Simpson WA, Younger JJ, Baddour LM, Barrett FF, Melton DM, et al. Adherence of coagulase-negative staphylococci to plastic tissue culture plates: a quantitative model for the adherence of staphylococci to medical devices. J Clin Microbiol 1985; 22: 996-1006. (Pubitemid 16222727)
29. Mack D, Davies AP, Harris LG, Rohde H, Horstkotte MA, Knobloch JK. Microbial interactions in Staphylococcus epidermidis biofilms. Anal Bioanal Chem 2007; 387: 399-408. (Pubitemid 46067457)
30. Evans RC, Holmes CJ. Effect of vancomycin hydrochloride on Staphylococcus epidermidis biofilm associated with silicone elastomer. Antimicrob Agents Chemother 1987; 31: 889-94. (Pubitemid 17084045)
31. Baddour LM, Bettmann MA, Bolger AF, Epstein AE, Ferrieri P, Gerber MA, et al. Nonvalvular cardiovascular device-related infections. Clin Infect Dis 2004; 38: 1128-30. (Pubitemid 38951259)
32. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 1999; 37: 1771-6. (Pubitemid 29235221)
33. Presterl E, Suchomel M, Eder M, Reichmann S, Lassnigg A, Graninger W, et al. Effects of alcohols, povidone-iodine and hydrogen peroxide on biofilms of Staphylococcus epidermidis. J Antimicrob Chemother 2007; 60: 417-20. (Pubitemid 47243897)
34. Mulcahy H, Charron-Mazenod L, Lewenza S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog 2008; 4: e1000213.
35. Gao R, Stock AM. Biological insights from structures of twocomponent proteins. Annu Rev Microbiol 2009; 63: 133-54.
36. Wagner C, Saizieu Ad A, Schonfeld HJ, Kamber M, Lange R, Thompson CJ, et al. Genetic analysis and functional characterization of the Streptococcus pneumoniae vic operon. Infect Immun 2002; 70: 6121-8. (Pubitemid 35192702)
37. Bisicchia P, Noone D, Lioliou E, Howell A, Quigley S, Jensen T, et al. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol Microbiol 2007; 65: 180-200. (Pubitemid 46938543)
38. Dubrac S, Msadek T. Identification of genes controlled by the essential YycG/YycF two-component system of Staphylococcus aureus. J Bacteriol 2004; 186: 1175-81. (Pubitemid 38209478)
39. Howell A, Dubrac S, Andersen KK, Noone D, Fert J, Msadek T, et al. Genes controlled by the essential YycG/YycF two-component system of Bacillus subtilis revealed through a novel hybrid regulator approach. Mol Microbiol 2003; 49: 1639-55. (Pubitemid 37153522)
40. Liu M, Hanks TS, Zhang J, McClure MJ, Siemsen DW, Elser JL, et al. Defects in ex vivo and in vivo growth and sensitivity to osmotic stress of group A Streptococcus caused by interruption of response regulator gene vicR. Microbiology 2006; 152: 967-78.
41. Ng WL, Robertson GT, Kazmierczak KM, Zhao J, Gilmour R, Winkler ME. Constitutive expression of PcsB suppresses the requirement for the essential VicR (YycF) response regulator in Streptococcus pneumoniae R6. Mol Microbiol 2003; 50: 1647-63. (Pubitemid 38010459)
42. Ng WL, Tsui HC, Winkler ME. Regulation of the pspA virulence factor and essential pcsB murein biosynthetic genes by the phosphorylated VicR (YycF) response regulator in Streptococcus pneumoniae. J Bacteriol 2005; 187: 7444-59. (Pubitemid 41507801)
43. Mohedano ML, Overweg K, de la Fuente A, Reuter M, Altabe S, Mulholland F, et al. Evidence that the essential response regulator YycF in Streptococcus pneumoniae modulates expression of fatty acid biosynthesis genes and alters membrane composition. J Bacteriol 2005; 187: 2357-67. (Pubitemid 40389134)
44. Ahn SJ, Wen ZT, Burne RA. Effects of oxygen on virulence traits of Streptococcus mutans. J Bacteriol 2007; 189: 8519-27. (Pubitemid 350210021)
45. Kadioglu A, Echenique J, Manco S, Trombe MC, Andrew PW. The MicAB two-component signaling system is involved in virulence of Streptococcus pneumoniae. Infect Immun 2003; 71: 6676-9. (Pubitemid 37337734)
46. Senadheera MD, Guggenheim B, Spatafora GA, Huang YC, Choi J, Hung DC, et al. A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 2005; 187: 4064-76. (Pubitemid 40827790)
47. Ahn SJ, Burne RA. Effects of oxygen on biofilm formation and the AtlA autolysin of Streptococcus mutans. J Bacteriol 2007; 189: 6293-302. (Pubitemid 47378637)
48. Shemesh M, Tam A, Feldman M, Steinberg D. Differential expression profiles of Streptococcus mutans ftf, gtf and vicR genes in the presence of dietary carbohydrates at early and late exponential growth phases. Carbohydr Res 2006; 341: 2090-7.
49. Gilmour R, Foster JE, Sheng Q, McClain JR, Riley A, Sun PM, et al. New class of competitive inhibitor of bacterial histidine kinases. J Bacteriol 2005; 187: 8196-200. (Pubitemid 41691714)
50. Kitayama T, Iwabuchi R, Minagawa S, Sawada S, Okumura R, Hoshino K, et al. Synthesis of a novel inhibitor against MRSA and VRE: preparation from zerumbone ring opening material showing histidinekinase inhibition. Bioorg Med Chem Lett 2007; 17: 1098-101. (Pubitemid 46177602)
51. Okada A, Gotoh Y, Watanabe T, Furuta E, Yamamoto K, Utsumi R. Targeting two-component signal transduction: a novel drug discovery system. Methods Enzymol 2007; 422: 386-95. (Pubitemid 47030660)
52. Stephenson K, Hoch JA. Developing inhibitors to selectively target two-component and phosphorelay signal transduction systems of pathogenic microorganisms. Curr Med Chem 2004; 11: 765-73. (Pubitemid 38380050)
53. Khardori N, Yassien M, Wilson K. Tolerance of Staphylococcus epidermidis grown from indwelling vascular catheters to antimicrobial agents. J Ind Microbiol 1995; 15: 148-51.