Novel strategy for biofilm inhibition by using small molecules targeting molecular chaperone DnaK

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 1, 2015, Pages 633-641

  Arita Morioka, Ken Ichi ^a   Yamanaka, Kunitoshi ^a   Mizunoe, Yoshimitsu ^b   Ogura, Teru ^a   Sugimoto, A Shinya ^b  

^a KUMAMOTO UNIVERSITY   (Japan)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; MYRICETIN; PANCURONIUM BROMIDE; PROTEIN DNAK; SIGMA FACTOR RPON; TELMISARTAN; VANCOMYCIN; ZAFIRLUKAST; BENZIMIDAZOLE DERIVATIVE; BENZOIC ACID DERIVATIVE; DNAK PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; FLAVONOID; HEAT SHOCK PROTEIN 70; PANCURONIUM; TOLUENESULFONIC ACID DERIVATIVE;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BIOFILM; CELL DIVISION; CELL FUNCTION; CELL MEMBRANE; COMPLEX FORMATION; CONCENTRATION RESPONSE; CYTOPLASM; ESCHERICHIA COLI K 12; HEAT SENSITIVITY; HEAT STRESS; IC50; NONHUMAN; PHENOTYPE; PROTEIN TARGETING; STAPHYLOCOCCUS AUREUS; TRANSMISSION ELECTRON MICROSCOPY; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; ESCHERICHIA COLI; GENETICS; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULARLY TARGETED THERAPY; PHYSIOLOGY;

BENZIMIDAZOLES; BENZOATES; BIOFILMS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLAVONOIDS; HSP70 HEAT-SHOCK PROTEINS; INHIBITORY CONCENTRATION 50; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR CHAPERONES; MOLECULAR TARGETED THERAPY; PANCURONIUM; STAPHYLOCOCCUS AUREUS; TOSYL COMPOUNDS; VANCOMYCIN;

EID: 84920170415     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.04465-14     Document Type: Article

References (61)

1. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx .doi.org/10.1126/science.284.5418.1318.
2. De Pozo JL, Patel R. 2009. Clinical practice. Infection associated with prosthetic joints. N Engl J Med 361:787-794. http://dx.doi.org/10.1056 /NEJMcp0905029.
3. Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol 8:623-633. http://dx.doi.org/10.1038/nrmicro2415.
4. Mika F, Hengge R. 2014. Small RNAs in the control of RpoS, CsgD, and biofilm architecture of Escherichia coli. RNA Biol 11:494-507. http://dx .doi.org/10.4161/rna.28867.
5. Kolodkin-Gal I, Romero D, Cao S, Clardy J, Kolter R, Losick R. 2010. D-Amino acids trigger biofilm disassembly. Science 328:627-629. http: //dx.doi.org/10.1126/science.1188628.
6. Boles BR, Horswill AR. 2008. agr-mediated dispersal of Staphylococcus aureus biofilms. PLoS Pathog 4:e1000052. http://dx.doi.org/10.1371 /journal.ppat.1000052.
7. Periasamy S, Joo HS, Duong AC, Bach TH, Tan VY, Chatterjee SS, Cheung GY, Otto M. 2012. How Staphylococcus aureus biofilms develop their characteristic structure. Proc Natl Acad Sci U S A 109:1281-1286. http://dx.doi.org/10.1073/pnas.1115006109.
8. Pratt LA, Kolter R. 1999. Genetic analyses of bacterial biofilm formation. Curr Opin Microbiol 12:598-603.
9. Danese PN, Pratt LA, Kolter R. 2000. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J Bacteriol 182:3593-3596. http://dx.doi.org/10.1128/JB.182.12.3593-3596 .2000.
10. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. 2001. The multicellular morphotypes of Salmonella Typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 39:1452-1463. http://dx.doi.org/10.1046/j.1365-2958 .2001.02337.x.
11. Itoh Y, Wang X, Hinnebusch BJ, Preston JF, III, Romeo T. 2005. Depolymerization of beta-1,6-N-acetyl-D-glucosamine disrupts the integrity of diverse bacterial biofilms. J Bacteriol 187:382-387. http://dx.doi .org/10.1128/JB.187.1.382-387.2005.
12. Kai-Larsen Y, Lüthje P, Chromek M, Peters V, Wang X, Holm A, Kádas L, Hedlund KO, Johansson J, Chapman MR, Jacobson SH, Römling U, Agerberth B, Brauner A. 2000. Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37. PLoS Pathog 6:e1001010. http://dx.doi.org/10.1371 /journal.ppat.1001010.
13. Bian Z, Brauner A, Li Y, Normark S. 2000. Expression of and cytokine activation by Escherichia coli curli fibers in human sepsis. J Infect Dis 181:602-612. http://dx.doi.org/10.1086/315233.
14. Kudinha T, Johnson JR, Andrew SD, Kong F, Anderson P, Gilbert GL. 2013. Genotypic and phenotypic characterization of Escherichia coli isolates from children with urinary tract infection and from healthy carriers. Pediatr Infect Dis J 32:543-548. http://dx.doi.org/10.1097/INF .0b013e31828ba3f1.
15. Blanco LP, Evans ML, Smith DR, Badtke MP, Chapman MR. 2012. Diversity, biogenesis and function of microbial amyloids. Trends Microbiol 20:66-73. http://dx.doi.org/10.1016/j.tim.2011.11.005.
16. Hammer ND, Schmidt JC, Chapman MR. 2007. The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization. Proc Natl Acad Sci U S A 104:12494-12499. http://dx.doi .org/10.1073/pnas.0703310104.
17. Hammar M, Arnqvist A, Bian Z, Olsén A, Normark S. 1995. Expression of two csg operons is required for production of fibronectin- and Congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 18: 661-670. http://dx.doi.org/10.1111/j.1365-2958.1995.mmi-18040661.x.
18. Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U. 2010. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar Typhimurium. J Bacteriol 192:456-466. http://dx.doi.org/10 .1128/JB.01826-08.
19. Mayer MP, Bukau B. 1998. Hsp70 chaperone systems: diversity of cellular functions and mechanism of action. Biol Chem 379:261-268.
20. Gässler CS, Buchberger A, Laufen T, Mayer MP, Schröder H, Valencia A, Bukau B. 1998. Mutations in the DnaK chaperone affecting interaction with the DnaJ cochaperone. Proc Natl Acad Sci U S A 95:15229-15234. http://dx.doi.org/10.1073/pnas.95.26.15229.
21. Laufen T, Mayer MP, Beisel C, Klostermeier D, Mogk A, Reinstein J, Bukau B. 1999. Mechanism of regulation of Hsp70 chaperones by DnaJ cochaperones. Proc Natl Acad Sci U S A 96:5452-5457. http://dx.doi.org /10.1073/pnas.96.10.5452.
22. Harrison CJ, Hayer-Hartl M, Di Liberto M, Hartl F, Kuriyan J. 1997. Crystal structure of the nucleotide exchange factor GrpE bound to the ATPase domain of the molecular chaperone DnaK. Science 276:431-435. http://dx.doi.org/10.1126/science.276.5311.431.
23. Langer T, Lu C, Echols H, Flanagan J, Hayer MK, Hartl FU. 1992. Successive action of DnaK, DnaJ and GroEL along the pathway of chap-erone-mediated protein folding. Nature 356:683-689. http://dx.doi.org /10.1038/356683a0.
24. Bukau B. 1993. Regulation of the Escherichia coli heat-shock response. Mol Microbiol 9:671-680. http://dx.doi.org/10.1111/j.1365-2958.1993 .tb01727.x.
25. Yura T, Nagai H, Mori H. 1993. Regulation of the heat-shock response in bacteria. Annu Rev Microbiol 47:321-350. http://dx.doi.org/10.1146 /annurev.mi.47.100193.001541.
26. Bukau B, Walker GC. 1989. Cellular defects caused by deletion of the Escherichia coli dnaK gene indicate roles for heat shock protein in normal metabolism. J Bacteriol 171:2337-2346.
27. Shi W, Zhou Y, Wild J, Adler J, Gross CA. 1992. DnaK, DnaJ, and GrpE are required for flagellum synthesis in Escherichia coli. J Bacteriol 174: 6256-6263.
28. Chakrabarti S, Sengupta N, Chowdhury R. 1999. Role of DnaK in in vitro and in vivo expression of virulence factors of Vibrio cholerae. Infect Immun 67:1025-1033.
29. Singh VK, Syring M, Singh A, Singhal K, Dalecki A, Johansson T. 2012. An insight into the significance of the DnaK heat shock system in Staphylococcus aureus. Int J Med Microbiol 302:242-252. http://dx.doi.org/10 .1016/j.ijmm.2012.05.001.
30. Lemos JA, Luzardo Y, Burne RA. 2007. Physiologic effects of forced down-regulation of dnaK and groEL expression in Streptococcus mutans. J Bacteriol 189:1582-1588. http://dx.doi.org/10.1128/JB.01655-06.
31. Niba ET, Naka Y, Nagase M, Mori H, Kitakawa M. 2007. A genomewide approach to identify the genes involved in biofilm formation in E. coli. DNA Res 14:237-246. http://dx.doi.org/10.1093/dnares/dsm024.
32. Rockabrand D, Livers K, Austin T, Kaiser R, Jensen D, Burgess R, Blum P. 1998. Roles of DnaK and RpoS in starvation-induced thermotolerance of Escherichia coli. J Bacteriol 180:846-854.
33. Niwa T, Ying BW, Saito K, Jin W, Takada S, Ueda T, Taguchi H. 2009. Bimodal protein solubility distribution revealed by an aggregation analysis of the entire ensemble of Escherichia coli proteins. Proc Natl Acad Sci U S A 106:4201-4206. http://dx.doi.org/10.1073/pnas.0811922106.
34. Sugimoto S, Yamanaka K, Nishikori S, Miyagi A, Ando T, Ogura T. 2010. AAA+ chaperone ClpX regulates dynamics of prokaryotic cytoskeletal protein FtsZ. J Biol Chem 285:6648-6657. http://dx.doi.org/10.1074 /jbc.M109.080739.
35. Tatsuta T, Tomoyasu T, Bukau B, Kitagawa M, Mori H, Karata K, Ogura T. 1998. Heat shock regulation in the ftsH null mutant of Escherichia coli: dissection of stability and activity control mechanisms of sigma32 in vivo. Mol Microbiol 30:583-593. http://dx.doi.org/10.1046/j .1365-2958.1998.01091.x.
36. Chiba A, Sugimoto S, Sato F, Hori S, Mizunoe Y. 23 August 2014. A refined technique for extraction of extracellular matrices from bacterial biofilms and its applicability. Microb Biotechnol http://dx.doi.org/10 .1111/1751-7915.12155.
37. Cegelski L, Pinkner JS, Hammer ND, Cusumano CK, Hung CS, Chorell E, Aberg V, Walker JN, Seed PC, Almqvist F, Chapman MR, Hultgren SJ. 2009. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 5:913-919. http://dx.doi.org /10.1038/nchembio.242.
38. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2:2006.0008. http://dx.doi.org/10.1038/msb4100050.
39. Cesa LC, Patury S, Komiyama T, Ahmad A, Zuiderweg ER, Gestwicki JE. 2013. Inhibitors of difficult protein-protein interactions identified by high-throughput screening of multiprotein complexes. ACS Chem Biol 8:1988-1997. http://dx.doi.org/10.1021/cb400356m.
40. Chang L, Miyata Y, Ung PM, Bertelsen EB, McQuade TJ, Carlson HA, Zuiderweg ER, Gestwicki JE. 2011. Chemical screens against a reconstituted multiprotein complex: myricetin blocks DnaJ regulation of DnaK through an allosteric mechanism. Chem Biol 18:210-221. http://dx.doi .org/10.1016/j.chembiol.2010.12.010.
41. Itikawa H, Ryu J. 1979. Isolation and characterization of a temperaturesensitive dnaK mutant of Escherichia coli B. J Bacteriol 138:339-344.
42. Paek KH, Walker GC. 1987. Escherichia coli dnaK null mutants are inviable at high temperature. J Bacteriol 169:283-290.
43. Sugimoto S, Saruwatari K, Higashi C, Sonomoto K. 2008. The proper ratio of GrpE to DnaK is important for protein quality control by the DnaK-DnaJ-GrpE chaperone system and for cell division. Microbiology 154:1876-1885. http://dx.doi.org/10.1099/mic.0.2008/017376-0.
44. Ma X, Ehrhardt DW, Margolin W. 1996. Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci U S A 93: 12998-13003. http://dx.doi.org/10.1073/pnas.93.23.12998.
45. Vida TA, Emr SD. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128:779-792. http: //dx.doi.org/10.1083/jcb.128.5.779.
46. Sheldrick GM, Jones PG, Kennard O, Williams DH, Smith GA. 1978. Structure of vancomycin and its complex with acetyl-D-alanyl-D-alanine. Nature 271:223-225. http://dx.doi.org/10.1038/271223a0.
47. Marrie TJ, Costerton JW. 1984. Scanning and transmission electron microscopy of in situ bacterial colonization of intravenous and intraarterial catheters. J Clin Microbiol 19:687-693.
48. Kaplan JB, Velliyagounder K, Ragunath C, Rohde H, Mack D, Knobloch JK, Ramasubbu N. 2004. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol 186:8213-8220. http://dx.doi.org/10.1128/JB.186.24.8213-8220.2004.
49. Dubin G, Chmiel D, Mak P, Rakwalska M, Rzychon M, Dubin A. 2001. Molecular cloning and biochemical characterisation of proteases from Staphylococcus epidermidis. Biol Chem 382:1575-1582. http://dx.doi.org /10.1515/BC.2001.192.
50. Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. 2002. Extracellular DNA required for bacterial biofilm formation. Science 295:1487. http://dx.doi.org/10.1126/science.295.5559.1487.
51. Cusumano CK, Pinkner JS, Han Z, Greene SE, Ford BA, Crowley JR, Henderson JP, Janetka JW, Hultgren SJ. 2011. Treatment and prevention of urinary tract infection with orally active FimH inhibitors. Sci Transl Med 3:109ra115. http://dx.doi.org/10.1126/scitranslmed.3003021.
52. Lo AW, Van de Water K, Gane PJ, Chan AW, Steadman D, Waksman G, Remaut H. 2014. Suppression of type 1 pilus assembly in uropathogenic Escherichia coli by chemical inhibition of subunit polymerization. J Antimicrob Chemother 69:1017-1026. http://dx.doi.org/10.1093/jac /dkt467.
53. Andersson EK, Bengtsson C, Evans ML, Chorell E, Sellstedt M, Lindgren AE, Hufnagel DA, Bhattacharya M, Tessier PM, Wittung-Stafshede P, Almqvist F, Chapman MR. 2013. Modulation of curli assembly and pellicle biofilm formation by chemical and protein chaperones. Chem Biol 20:1245-1254. http://dx.doi.org/10.1016/j.chembiol .2013.07.017.
54. de la Fuente-Núñez C, Reffuveille F, Haney EF, Straus SK, Hancock RE. 2014. Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog 10:e1004152. http://dx.doi.org/10.1371/journal .ppat.1004152.
55. Sugimoto S, Mahin A, Sonomoto K. 2008. Molecular chaperones in lactic acid bacteria: physiological consequences and biochemical properties. J Biosci Bioeng 106:324-336. http://dx.doi.org/10.1263/jbb.106.324.
56. Bigger JW. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244:497-500. http://dx.doi.org/10 .1016/S0140-6736(00)74210-3.
57. Conlon BP, Nakayasu ES, Fleck LE, LaFleur MD, Isabella VM, Coleman K, Leonard SN, Smith RD, Adkins JN, Lewis K. 2013. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 503:365-370. http://dx.doi.org/10.1038/nature12790.
58. Hansen S, Lewis K, Vulić M. 2008. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob Agents Chemother 52:2718-2726. http://dx.doi.org/10.1128 /AAC.00144-08.
59. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ. 2002. B modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184:5457-5467. http://dx.doi.org/10.1128/JB .184.19.5457-5467.2002.
60. Sugimoto S, Iwase T, Sato F, Tajima A, Shinji H, Mizunoe Y. 2011. Cloning, expression and purification of extracellular serine protease Esp, a biofilm-degrading enzyme, from Staphylococcus epidermidis. J Appl Microbiol 111:1406-1415. http://dx.doi.org/10.1111/j.1365-2672 .2011.05167.x.
61. Kreiswirth BN, Löfdahl S, Betley MJ, O'Reilly M, Schlievert PM, Bergdoll MS, Novick RP. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-712. http://dx.doi.org/10.1038/305709a0.