Advertisement

Sodium houttuyfonate in vitro inhibits biofilm dispersion and expression of bdlA in Pseudomonas aeruginosa

  • Tianming Wang
  • Weifeng Huang
  • Qiangjun Duan
  • Jian Wang
  • Huijuan Cheng
  • Jing Shao
  • Fang Li
  • Daqiang Wu
Original Article

Abstract

Biofilm dispersion is the last step in the development of biofilms, and allows bacteria to spawn novel biofilms in new locales. In the previous studies, we found that sodium houttuyfonate (SH) is effective at inhibiting biofilm formation and motility of Pseudomonas aeruginosa. Here, we investigated the effect of SH against the biofilm dispersion of P. aeruginosa by an in vitro model. The results show that the plant derivative, SH, could effectively inhibit both biofilm dispersion of P. aeruginosa, and gene and protein expression of the key biofilm regulator BdlA in a dose-dependent manner. Furthermore, our presented results suggest that SH can penetrate into the biofilm of P. aeruginosa to repress the biofilm life cycle. Therefore, these results indicate that the antimicrobial activity of SH may be partially due to its ability to disrupt biofilm dispersion in P. aeruginosa.

Keywords

Sodium houttuyfonate Traditional medicine Biofilm dispersion Pseudomonas aeruginosa BdlA 

Notes

Acknowledgements

This work was supported by and key discipline of Anhui University of Chinese Medicine and the National Natural Science Foundation of China (Grant Nos. 81503115, 81603167, 81573725). The authors are grateful for Prof Huang in Anhui University of Chinese Medicine for suggestions on immunoblotting assay.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interests.

References

  1. 1.
    Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79CrossRefPubMedGoogle Scholar
  3. 3.
    Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2:114–122CrossRefPubMedGoogle Scholar
  4. 4.
    Harmsen M, Yang L, Pamp SJ, Tolker-Nielsen T (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59:253–268CrossRefPubMedGoogle Scholar
  5. 5.
    Solano C, Echeverz M, Lasa I (2014) Biofilm dispersion and quorum sensing. Curr Opin Microbiol 18:96–104CrossRefPubMedGoogle Scholar
  6. 6.
    Barraud N, Schleheck D, Klebensberger J et al (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191:7333–7342CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Liu G, Xiang H, Tang X et al (2011) Transcriptional and functional analysis shows sodium houttuyfonate-mediated inhibition of autolysis in Staphylococcus aureus. Molecules 16:8848–8865CrossRefPubMedGoogle Scholar
  8. 8.
    Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P (2004) Characterization of nutrient-induced dispersion in Pseudomonas aeruginosa PAO1 biofilm. J Bacteriol 186:7312–7326CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Driscoll JA, Brody SL, Kollef MH (2007) The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 67:351–368CrossRefPubMedGoogle Scholar
  11. 11.
    Breidenstein EB, de la Fuente-Nunez C, Hancock RE (2011) Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 19:419–426CrossRefPubMedGoogle Scholar
  12. 12.
    Morita Y, Tomida J, Kawamura Y (2014) Responses of Pseudomonas aeruginosa to antimicrobials. Front Microbiol 4:422CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Li Y, Petrova OE, Su S et al (2014) BdlA, DipA and induced dispersion contribute to acute virulence and chronic persistence of Pseudomonas aeruginosa. PLoS Pathog 10:e1004168CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Morgan R, Kohn S, Hwang SH, Hassett DJ, Sauer K (2006) BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol 188:7335–7343CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Deng ZP, Zhong DF, Meng J, Chen XY (2012) Covalent protein binding and tissue distribution of houttuynin in rats after intravenous administration of sodium houttuyfonate. Acta Pharmacol Sin 33:568–576CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Petrova OE, Sauer K (2012) Dispersion by Pseudomonas aeruginosa requires an unusual posttranslational modification of BdlA. Proc Natl Acad Sci USA 109:16690–16695CrossRefPubMedGoogle Scholar
  17. 17.
    Petrova OE, Sauer K (2012) PAS domain residues and prosthetic group involved in BdlA-dependent dispersion response by Pseudomonas aeruginosa biofilms. J Bacteriol 194:5817–5828CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Rahmani-Badi A, Sepehr S, Fallahi H, Heidari-Keshel S (2015) Dissection of the cis-2-decenoic acid signaling network in Pseudomonas aeruginosa using microarray technique. Front Microbiol 6:383PubMedPubMedCentralGoogle Scholar
  19. 19.
    Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5:e1000483CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Sharma G, Rao S, Bansal A, Dang S, Gupta S, Gabrani R (2014) Pseudomonas aeruginosa biofilm: potential therapeutic targets. Biologicals 42:1–7CrossRefPubMedGoogle Scholar
  21. 21.
    Gao JP, Chen CX, Wang Y, Lu J, Gu WL (2009) Effect of sodium houttuyfonate on myocardial hypertrophy in mice and rats. J Pharm Pharmacol 61:677–683CrossRefPubMedGoogle Scholar
  22. 22.
    Gao JP, Chen CX, Wu Q, Gu WL, Li X (2010) Effect of sodium houttuyfonate on inhibiting ventricular remodeling induced by abdominal aortic banding in rats. Can J Physiol Pharmacol 88:693–701CrossRefPubMedGoogle Scholar
  23. 23.
    Wang D, Yu Q, Eikstadt P, Hammond D, Feng Y, Chen N (2002) Studies on adjuvanticity of sodium houttuyfonate and its mechanism. Int Immunopharmacol 2:1411–1418CrossRefPubMedGoogle Scholar
  24. 24.
    Shao J, Cheng H, Wang C, Wang Y (2012) A phytoanticipin derivative, sodium houttuyfonate, induces in vitro synergistic effects with levofloxacin against biofilm formation by Pseudomonas aeruginosa. Molecules 17:11242–11254CrossRefPubMedGoogle Scholar
  25. 25.
    Shao J, Cheng H, Wang C et al (2013) Sodium houttuyfonate, a potential phytoanticipin derivative of antibacterial agent, inhibits bacterial attachment and pyocyanine secretion of Pseudomonas aeruginosa by attenuating flagella-mediated swimming motility. World J Microbiol Biotechnol 29:2373–2378CrossRefPubMedGoogle Scholar
  26. 26.
    Shao J, Cheng H, Wu D et al (2013) Antimicrobial effect of sodium houttuyfonate on Staphylococcus epidermidis and Candida albicans biofilms. J Tradit Chin Med 33:798–803CrossRefPubMedGoogle Scholar
  27. 27.
    Wu DQ, Huang WF, Duan QJ, Cheng HJ (2015) Sodium houttuyfonate inhibits biofilm formation and alginate biosynthesis-associated gene expression in a clinical strain of Pseudomonas aeruginosa in vitro. Exp Ther Med 10:753–758CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Wu DQ, Huang WF, Duan QJ, Cheng HJ, Wang CZ (2015) Sodium houttuyfonate inhibits virulence related motility of Pseudomonas aeruginosa. Zhongguo Zhong Yao Za Zhi 40:1585–1588PubMedGoogle Scholar
  29. 29.
    Huang W, Duan Q, Li F, Shao J, Cheng H, Wu D (2015) Sodium houttuyfonate and EDTA-Na(2) in combination effectively inhibits Pseudomonas aeruginosa, Staphylococcus aureus and Candida albicans in vitro and in vivo. Bioorg Med Chem Lett 25:142–147CrossRefPubMedGoogle Scholar
  30. 30.
    Wu D, Huang W, Duan Q, Li F, Cheng H (2014) Sodium houttuyfonate affects production of N-acyl homoserine lactone and quorum sensing-regulated genes expression in Pseudomonas aeruginosa. Front Microbiol 5:635PubMedPubMedCentralGoogle Scholar
  31. 31.
    Imperi F, Leoni L, Visca P (2014) Antivirulence activity of azithromycin in Pseudomonas aeruginosa. Front Microbiol 5:178CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Tan H, Zhang L, Weng Y et al (2016) PA3297 counteracts antimicrobial effects of azithromycin in Pseudomonas aeruginosa. Front Microbiol 7:317PubMedPubMedCentralGoogle Scholar
  33. 33.
    Shao J, Lu K, Tian G et al (2015) Lab-scale preparations of Candida albicans and dual Candida albicans-Candida glabrata biofilms on the surface of medical-grade polyvinyl chloride (PVC) perfusion tube using a modified gravity-supported free-flow biofilm incubator (GS-FFBI). J Microbiol Methods 109:41–48CrossRefPubMedGoogle Scholar
  34. 34.
    Savli H, Karadenizli A, Kolayli F, Gundes S, Ozbek U, Vahaboglu H (2003) Expression stability of six housekeeping genes: a proposal for resistance gene quantification studies of Pseudomonas aeruginosa by real-time quantitative RT-PCR. J Med Microbiol 52:403–408CrossRefPubMedGoogle Scholar
  35. 35.
    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 25:402–408CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Kohler T, Dumas JL, Van Delden C (2007) Ribosome protection prevents azithromycin-mediated quorum-sensing modulation and stationary-phase killing of Pseudomonas aeruginosa. Antimicrob Agents Chemother 51:4243–4248CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Lovmar M, Tenson T, Ehrenberg M (2004) Kinetics of macrolide action: the josamycin and erythromycin cases. J Biol Chem 279:53506–53515CrossRefPubMedGoogle Scholar
  39. 39.
    Starosta AL, Karpenko VV, Shishkina AV et al (2010) Interplay between the ribosomal tunnel, nascent chain, and macrolides influences drug inhibition. Chem Biol 17:504–514CrossRefPubMedGoogle Scholar
  40. 40.
    Wood TK (2014) Biofilm dispersal: deciding when it is better to travel. Mol Microbiol 94:747–750CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Tianming Wang
    • 1
    • 2
  • Weifeng Huang
    • 1
    • 2
  • Qiangjun Duan
    • 1
    • 2
  • Jian Wang
    • 4
  • Huijuan Cheng
    • 1
    • 2
  • Jing Shao
    • 1
    • 2
  • Fang Li
    • 1
    • 3
  • Daqiang Wu
    • 1
    • 2
  1. 1.Laboratory of Microbiology and Immunology, School of Chinese and Western Integrative MedicineAnhui University of Chinese MedicineHefeiChina
  2. 2.Institute of Chinese and Western Medicine ResearchAnhui Academy of Chinese MedicineHefeiChina
  3. 3.National Chinese Medicinal Material Product Quality Supervision and Inspection Center (Anhui)BozhouChina
  4. 4.Pathology DepartmentFirst Affiliated Hospital of Anhui University of Chinese MedicineHefeiChina

Personalised recommendations