Biofilm prevention by dicephalic cationic surfactants and their interactions with DNA

Journal of Applied Microbiology

Volumn 121, Issue 3, 2016, Pages 682-692

  Piecuch, A ^a   Lamch, L ^b   Paluch, E ^a   Oblak E ^a   Wilk, K A ^b  

^a UNIVERSITY OF WROC AW   (Poland)

^b WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

adhesion; biofilm; dicephalic cationic surfactants; disinfectants; DNA complexation

Indexed keywords

ADHESION; BACTERIA; BIOFILMS; DNA; DYES;

ANTIBACTERIALS; BACTERIAL ADHESION; DIBROMIDES; DICEPHALIC CATIONIC SURFACTANT; DICEPHALIC SURFACTANTS; DIMETHYLAMINES; DNA COMPLEXATION; EPIDERMIDIS; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS EPIDERMIDIS;

CATIONIC SURFACTANTS;

ANTIBIOTIC AGENT; BACTERIAL DNA; CATIONIC SURFACTANT; COUNTERION; CRYSTAL VIOLET; ETHIDIUM BROMIDE; GLASS; HYDROCARBON; N,N BIS[3,3' (TRIMETHYLAMMONIO)PROPYL]ALKYLAMIDE DIBROMIDE DERIVATIVE; N,N' BIS[3,3' (DIMETHYLAMINE)PROPYL]ALKYLAMIDE DERIVATIVE; STAINLESS STEEL; UNCLASSIFIED DRUG;

ADHESION; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; CATION; CONCENTRATION (COMPOSITION); DISINFECTION; DNA; INHIBITION; SURFACTANT;

ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COUNT; BACTERIUM ADHERENCE; BIOFILM; CONTROLLED STUDY; DRUG DNA INTERACTION; DRUG SCREENING; DRUG SYNTHESIS; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PSEUDOMONAS AERUGINOSA; STAINING; STAPHYLOCOCCUS EPIDERMIDIS; STRUCTURE ACTIVITY RELATION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84982113758     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.13204     Document Type: Article

References (58)

1. Alipour, M., Omri, A. and Suntres, Z.E. (2011) Ginseng aqueous extract attenuates the production of virulence factors, stimulates twitching and adhesion, and eradicates biofilms of Pseudomonas aeruginosa. Can J Physiol Pharmacol 89, 419–427.
2. Bayoudh, S., Othmane, A., Bettaieb, F., Bakhrouf, A., Ben Ouada, H. and Ponsonnet, L. (2006) Quantification of the adhesion free energy between bacteria and hydrophobic and hydrophilic substrata. Mater Sci Eng 26, 300–3005.
3. Bazylińska, U., Zieliński, W., Kulbacka, J., Samoć, M. and Wilk, K.A. (2016) New diamidequat-type surfactants in fabrication of long-sustained theranostic nanocapsules: colloidal stability, drug delivery and bioimaging. Colloids Surf B Biointerfaces 137, 121–132.
4. Begec, Z., Yucel, A., Yakupogullari, Y., Erdogan, M.A., Duman, Y., Durmus, M. and Ersoy, M.O. (2013) The antimicrobial effects of ketamine combined with propofol: an in vitro study. Rev Bras Anestesiol 63, 461–465.
5. Bhattacharya, S. and Bajaj, A. (2009) Advances in gene delivery through molecular design of cationic lipids. Chem Commun 16, 4632–4656.
6. Bhattacharya, S. and Samanta, S.K. (2011) Surfactants possessing multiple polar heads. A perspective on their unique aggregation behavior and applications. J Phys Chem Lett 2, 914–920.
7. Bridier, A., Briandet, R., Thomas, V. and Dubois-Brissonnet, F. (2011) Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27, 1017–1032.
8. Buttner, H., Mack, D. and Rohde, H. (2015) Structural basis of Staphylococcus epidermidis biofilm formation: mechanisms and molecular interactions. Front Cell Infect Microbiol 5, 14.
9. Cardoso, A.M., Faneca, H., Almeida, J.A., Pais, A.A., Marques, E.F., de Lima, M.C. and Jurado, A.S. (2011) Gemini surfactant dimethylene -1,2-bis (tetradecyl- dimethylammonium bromide)-based gene vectors: a biophysical approach to transfection efficiency. Biochim Biophys Acta 1808, 341–351.
10. Daniels, J.B., Scoffield, J., Woolnough, J.L. and Silo-Suh, L. (2014) Impact of glycerol-3-phosphate dehydrogenase on virulence factor production by Pseudomonas aeruginosa. Can J Microbiol 60, 857–863.
11. Deo, A.A., Kulkarni, A.S. and Meshram, S.U. (2010) Monocationic surfactant induced ultra-structural changes in antibiotic resistant Escherichia coli. Indian J Med Res 131, 825–828.
12. Frąckowiak, R., Para, G., Warszyński, P. and Wilk, K.A. (2012a) New environmentally friendly dicephalic amine dichlorides; nonequivalent adsorption and interactions with model polyelectrolyte. Colloids Surf A Physicochem Eng Asp 413, 108–114.
13. Frąckowiak, R., Piasecki, A. and Wilk, K.A. (2012b). New Surface Active Aliphatic Amides Dihydrochlorides, derivatives of 3,30-iminobis(n,n-dimethylpropylamine) and method of their production. Patent PL 211591.
14. Frąckowiak, R., Piasecki, A. and Wilk, K.A. (2012c) Bis-ammonium aliphatic salts of 3,30-iminobis(n, n-dimethylpropylamine) and method of their production. Patent PL 211857.
15. Gallardo-Moreno, A.M., Gonzales-Martin, M.L., Perez-Giraldo, C., Garduno, E., Bruque, J.M. and Gomez-Garcia, A.C. (2002) Thermodynamic analysis of growth temperature dependence in the adhesion of Candida parapsilosis to polystyrene. Appl Environ Microbiol 68, 2610–2613.
16. Grenier, M.C., Davis, R.W., Wilson-Henjum, K.L., LaDow, J.E., Black, J.W., Caran, K.L., Seifert, K. and Minbiole, K.P.C. (2012) The antibacterial activity of 4,4′-bipyridinium amphiphiles with conventional, d icephalic and gemini architectures. Bioorg Med Chem Lett 22, 4055–4058.
17. Haldar, J., Kondaiah, P. and Bhattacharya, S. (2005) Synthesis and antibacterial properties of novel hydrolyzable cationic amphiphiles. incorporation of multiple head groups leads to impressive antibacterial activity. J Med Chem 48, 3823–3831.
18. Harmsen, M., Yang, L., Pamp, S.J. and Tolker-Nielsen, T. (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59, 253–268.
19. Hegstad, K., Langsrud, S., Lunestad, B.T., Scheie, A.A., Sunde, M. and Yazdankhah, S.P. (2010) Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb Drug Resist 16, 91–104.
20. Ioannou, C.J., Hanlon, G.W. and Denyer, S.P. (2007) Action of disinfectant quaternary ammonium compounds against Staphylococcus aureus. Antimicrob Agents Chemother 51, 296–306.
21. Jaramillo, D.E., Arriola, A., Safavi, C. and Chavez de Paz, L.E. (2012) Decreased bacterial adherence and biofilm growth on surfaces coated with a solution of benzalkonium chloride. J Endod 38, 821–825.
22. Jimenez, P., Koch, G., Thompson, J., Xavier, K., Cool, R. and Quax, W. (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76, 46–65.
23. Kim, H.S. and Park, H.D. (2013) Ginger extract inhibits biofilm formation by Pseudomonas aeruginosa PA14. PLoS ONE 8, e76106.
24. Kostakioti, M., Hadjifrangiskou, M. and Hultgren, S.J. (2013) Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med 3, a010306.
25. Lellouche, J., Friedman, A., Gedanken, A. and Banin, E. (2012) Antibacterial and antibiofilm properties of yttrium fluoride nanoparticles. Int J Nanomedicine 7, 5611–5624.
26. Machado, I., Graca, J., Sousa, A.M., Lopes, S.P. and Pereira, M.O. (2011) Effect on antimicrobial residues on early adhesion and biofilm formation by wild-type and benzalkonium chloride-adapted Pseudomonas aeruginosa. Biofouling 27, 1151–1159.
27. Marsich, E., Travan, A., Donati, I., Turco, G., Kulkova, J., Moritz, N., Aro, H.T., Crosera, M. et al. (2013) Biological responses of silver-coated thermosets: an in vitro and in vivo study. Acta Biomater 9, 5088–5099.
28. Meekel, A.A.P., Wagenaar, A., Smisterová, J., Kroeze, J.E., Haadsma, P., Bosgraaf, B., Stuart, M.A., Brisson, A. et al. (2000) Synthesis of pyridinium amphiphiles used for transfection and some characteristics of amphiphile/DNA complex formation. Eur J Org Chem 2000, 665–673.
29. Meister, A. and Blume, A. (2007) Self-assembly of bipolar amphiphiles. Curr Opin Colloid Interface Sci 12, 138–147.
30. Mikkelsen, H., Sivaneson, M. and Filloux, A. (2011) Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol 13, 1666–1681.
31. Mukherji, R. and Prabhune, A. (2014) Novel glycolipids synthesized using plant essential oils and their application in quorum sensing inhibition and as antibiofilm agents. ScientificWorldJournal 2014, 890709.
32. Nan, L., Yang, K. and Ren, G. (2015) Anti-biofilm formation of a novel stainless steel against Staphylococcus aureus. Mater Sci Eng C Mater Biol Appl 51, 356–361.
33. National Committee for Clinical Laboratory Standards (2000) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved Standard – fifth edition, NCCLS document 20, M7-A5. Wayne, PA, USA: National Committee for Clinical Laboratory Standards.
34. Nejadnik, M.R., van der Mei, H.C., Norde, W. and Busscher, H.J. (2008) Bacterial adhesion and growth on a polymer brush-coating. Biomaterials 29, 4117–4121.
35. Obłąk, E., Piecuch, A., Krasowska, A. and Łuczyński, J. (2013) Antifungal activity of gemini quaternary ammonium salts. Microbiol Res 168, 630–638.
36. Obłąk, E., Piecuch, A., Dworniczek, E. and Olejniczak, T. (2014a) The influence of biodegradable gemini surfactants, N, N′-bis(1-decyloxy-1-oxopronan-2-yl)-N, N, N′, N′ tetramethyl- propane-1,3-diammonium dibromide and N, N′-bis(1-dodecyloxy-1-oxopronan -2-yl) N, N, N′, N′-tetramethylethane-1,2-diammonium dibromide, on fungal biofilm and adhesion. J Oleo Sci 64, 527–537.
37. Obłąk, E., Piecuch, A., Guz-Regner, K. and Dworniczek, E. (2014b) Antibacterial activity of gemini quaternary ammonium salts. FEMS Microbiol Lett 350, 190–198.
38. Otto, M. (2009) Staphylococcus epidermidis – the “accidental” pathogen. Nat Rev Microbiol 7, 555–567.
39. Paria, S. and Khilar, K.C. (2004) A review on experimental studies of surfactant adsorption at the hydrophilic solid-water interphase. Adv Colloid Interface Sci 110, 75–95.
40. Peng, L.Q., Zhong, L.J., Zhou, H.F., Wu, X.E. and Chen, X.D. (2015) Grafting of ionic liquids on stainless steel surface for antibacterial application. Colloids Surf B Biointerfaces 126, 162–168.
41. Piecuch, A., Obłąk, E. and Guz-Regner, K. (2016) Antibacterial activity of alanine-derived gemini quaternary ammonium compounds. J Surfactants Deterg 19, 275–282.
42. Piętka-Ottlik, M., Frąckowiak, R., Maliszewska, I., Kołwzan, B. and Wilk, K.A. (2012) Ecotoxicity and biodegradability of antielectrostatic dicephalic cationic surfactants. Chemosphere 89, 1103–1111.
43. Roe, D., Karandikar, B., Bonn-Savage, N., Gibbins, B. and Roullet, J.-B. (2008) Antimicrobial surface functionalization of plastic catheters by silver nanoparticles. J Antimicrob Chemother 61, 869–876.
44. Rybtke, M., Hultqvist, L.D., Givskov, M. and Tolker-Nielsen, T. (2015) Pseudomonas aeruginosa biofilm infections: community structure, antimicrobial tolerance and immune response. J Mol Biol 427, 3628–3645.
45. Ryhanen, S.J., Saily, M.J., Paukku, T., Borocci, S., Mancini, G., Holopainen, J.M. and Kinnunen, P.K. (2003) Surface charge density determines the efficiency of cationic gemini surfactant based lipofection. Biophys J 84, 578–587.
46. Saeidi, N., Wong, C., Lo, T.-M., Nguyen, H., Ling, H., Leong, S., Poh, C. and Chang, M. (2011) Engineering microbes to sense and eradicate Pseudomonas aeruginosa, a human pathogen. Mol Syst Biol 7, 1–11.
47. Scutera, S., Zucca, M. and Savoia, D. (2014) Novel approaches for the design and discovery of quorum-sensing inhibitors. Expert Opin Drug Discov 9, 353–366.
48. Shucla, D. and Tyagi, V.K. (2006) Cationic gemini surfactants: a review. J Oleo Sci 55, 381–390.
49. Skrzela, R., Para, G., Warszyński, P. and Wilk, K.A. (2010) Experimental and theoretical approach to nonequivalent adsorption of novel dicephalic ammonium surfactants at the air/solution interface. J Phys Chem B 114, 10471–10480.
50. Sriram, M.I., Kalishwaralal, K., Deepak, V., Gracerosepat, R., Srisakthi, K. and Gurunathan, S. (2011) Biofilm inhibition and antimicrobial action of lipopeptide biosurfactant produced by heavy metal tolerant strain Bacillus cereus NK1. Colloids Surf B Biointerfaces 85, 174–181.
51. Szczepanowicz, K., Bazylińska, B., Pietkiewicz, J., Szyk-Warszyńska, L., Wilk, K.A. and Warszyński, P. (2015) Biocompatible long-sustained release oil-core polyelectrolyte nanocarriers: from controlling physical state and stability to biological impact. Adv Colloid Interface Sci 222, 678–691.
52. Taguchi, F., Suzuki, T., Inagaki, Y., Toyoda, K., Shiraishi, T. and Ichinose, Y. (2010) The siderophore pyoverdine of Pseudomonas syringae pv. tabaci 6605 is an intrinsic virulence factor in host tobacco infection. J Bacteriol 192, 117–126.
53. Tangh, H., Cao, T., Liang, X., Wang, A., Salley, S.O., McAllister, J. 2nd and Ng, K.Y. (2009) Influence of silicone surface roughness and hydrophobicity on adhesion and colonization of Staphylococcus epidermidis. J Biomed Mater Res A 88, 454–463.
54. Tehrani-Bagha, A. and Holmberg, K. (2007) Cleavable surfactants. Curr Opin Colloid Interface Sci 12, 81–91.
55. Toba, F.A., Visai, L., Trivedi, S. and Lowy, F.D. (2013) The role of ionic interactions in the adherence of Staphylococcus epidermidis adhesion SdrF to prosthetic material. FEMS Microbiol Lett 338, 24–30.
56. Wang, J., Huang, N., Pan, C.J., Kwok, S.C.H., Yang, P., Leng, Y.X., Chen, J.Y., Sun, H. et al. (2004) Bacterial repellence from polyethylene terephthalate surface modified by acetylene plasma immersion ion implantation-deposition. Surf Coat Technol 186, 299–304.
57. Zana, R. (2002) Dimeric and oligomeric surfactants. Behavior at interfaces and in aqueous solution: a review. Adv Colloid Interface Sci 97, 205–253.
58. Zhang, L. (2003) Quorum quenching and proactive host defense. Trends Plant Sci 8, 238–244.