Skip to main content

Advertisement

Log in

Effect of curcumin on growth, biofilm formation and virulence factor gene expression of Porphyromonas gingivalis

  • Original Article
  • Published:
Odontology Aims and scope Submit manuscript

Abstract

Porphyromonas gingivalis is a keystone pathogen and major colonizer in host tissue which plays a pivotal role in periodontitis among the other polymicrobial infections. Increasing facts demonstrate that curcumin has antibacterial activity and anti-biofilm effect against the periodontopathogens through diverse mechanisms that have a positive impact on periodontal health. The present study was aimed to elucidate the effect of curcumin on biofilm formation and virulence factor gene expression of P. gingivalis. By using gene expression studies, we exploited the mechanism of anti-biofilm effects of curcumin on P. gingivalis. The minimum inhibitory concentration and minimum bactericidal concentration of curcumin for both ATCC and clinical strains of P. gingivalis were found to be 62.5 and 125 µg ml−1 respectively. Curcumin prevented bacterial adhesion and biofilm formation in a dose-dependent manner. Further, curcumin attenuated the virulence of P. gingivalis by reducing the expression of genes coding for major virulence factors, including adhesions (fimA, hagA, and hagB) and proteinases (rgpA, rgpB, and kgp). The results indicated that curcumin has shown anti-biofilm as well as antibacterial activity against P. gingivalis. Further, curcumin because of its pleiotropic actions could be a simple and inexpensive therapeutic strategy in the treatment of periodontal disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Shahzad M, Millhouse E, Culshaw S, Edwards CA, Ramage G, Combet E. Selected dietary (poly) phenols inhibit periodontal pathogen growth and biofilm formation. Food Funct. 2015;6(3):719–29. https://doi.org/10.1039/C4FO01087F.

    Article  PubMed  Google Scholar 

  2. Tonetti MS, Jepsen S, Jin L. Otomo-Corgel J Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: a call for global action. J Clin Periodontol. 2017;44(5):456–62. https://doi.org/10.1111/jcpe.12732.

    Article  PubMed  Google Scholar 

  3. Sakanaka A, Takeuchi H, Kuboniwa M, Amano A. Dual lifestyle of Porphyromonas gingivalis in biofilm and gingival cells. Microb Pathog. 2016;94:42–7. https://doi.org/10.1016/j.micpath.2015.10.003.

    Article  PubMed  Google Scholar 

  4. Kim J, Amar S. Periodontal disease and systemic conditions: a bidirectional relationship. Odontology. 2006;94(1):10–211. https://doi.org/10.1007/s10266-006-0060-6.

    Article  PubMed  PubMed Central  Google Scholar 

  5. How KY, Song KP, Chan KG. Porphyromonas gingivalis: an overview of periodontopathic pathogen below the gum line. Front Microbiol. 2016;7:53. https://doi.org/10.3389/fmicb.2016.00053.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Warinner C, Rodrigues JFM, Vyas R, Trachsel C, Shved N, Grossmann J, Radini A, Hancock Y, Tito RY, Fiddyment S, Speller C, et al. Pathogens and host immunity in the ancient human oral cavity. Nature Genet. 2014;46(4):336–44. https://doi.org/10.1038/ng.2906.

    Article  PubMed  Google Scholar 

  7. Pandit N, Changela R, Bali D, Tikoo P, Gugnani S. Porphyromonas gingivalis: its virulence and vaccine. J Int Clin Dent Res Org. 2015;7(1):51. https://doi.org/10.4103/2231-0754.153496.

    Article  Google Scholar 

  8. Connolly E, Millhouse E, Doyle R, Culshaw S, Ramage G, Moran GP. The Porphyromonas gingivalis hemagglutinins HagB and HagC are major mediators of adhesion and biofilm formation. Mol Oral Microbiol. 2017;32(1):35–47. https://doi.org/10.1111/omi.12151.

    Article  PubMed  Google Scholar 

  9. Li N, Collyer CA. Gingipains from Porphyromonas gingivalis-complex domain structures confer diverse functions. Eur J Microbiol Immunol. 2011;1(1):41–58. https://doi.org/10.1556/EuJMI.1.2011.1.7.

    Article  Google Scholar 

  10. Laheij AM, Van Loveren C, Deng D, de Soet JJ. The impact of virulence factors of Porphyromonas gingivalis on wound healing in vitro. J Oral Microbiol. 2015;7(1):27543. https://doi.org/10.3402/jom.v7.27543.

    Article  PubMed  Google Scholar 

  11. Tanwar J, Hungund S, Dodani K. Nonsurgical periodontal therapy: a review. J Oral Res Rew. 2016;8(1):39. https://doi.org/10.4103/2249-4987.182490.

    Article  Google Scholar 

  12. Slots J, Ting M. Systemic antibiotics in the treatment of periodontal disease. Periodontol 2000. 2000;28(1):106–76. https://doi.org/10.1034/j.1600-0757.2002.280106.x.

    Article  Google Scholar 

  13. Torwane NA, Hongal S, Goel P, Chandrashekar BR. Role of Ayurveda in management of oral health. Pharmacogn Rev. 2014;8(15):16–211. https://doi.org/10.4103/0973-7847.125518.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Peram MR, Jalalpure SS, Joshi SA, Palkar MB, Diwan PV. Single robust RP-HPLC analytical method for quantification of curcuminoids in commercial turmeric products, Ayurvedic medicines, and nanovesicular systems. J Liq Chromatogr Relat Technol. 2017;40(10):487–98. https://doi.org/10.1080/10826076.2017.1329742.

    Article  Google Scholar 

  15. Mandroli PS, Bhat K. An in-vitro evaluation of antibacterial activity of curcumin against common endodontic bacteria. J Appl Pharm Sci. 2013;3(10):106–8. https://doi.org/10.7324/JAPS.2013.31018.

    Article  Google Scholar 

  16. Li B, Li X, Lin H, Zhou Y. Curcumin as a promising antibacterial agent: effects on metabolism and biofilm formation in S. mutans. BioMed Res Int. 2018. https://doi.org/10.1155/2018/4508709.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Izui S, Sekine S, Maeda K, Kuboniwa M, Takada A, Amano A, Nagata H. Antibacterial activity of curcumin against periodontopathic bacteria. J Periodontol. 2016;87(1):83–90. https://doi.org/10.1902/jop.2015.150260.

    Article  PubMed  Google Scholar 

  18. Wayne PA Clinical and laboratory standards institute. Performance standards for antimicrobial susceptibility testing. Twenty-third informational supplement CLSI document, 2011; 33(1) CLSI: USA M100-S23, 2013

  19. Nalawade TM, Bhat KG, Sogi S. Antimicrobial activity of endodontic medicaments and vehicles using agar well diffusion method on facultative and obligate anaerobes. Int J Clin Pediatr Dent. 2016;9(4):335–41. https://doi.org/10.5005/jp-journals-10005-1388.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Kugaji MS, Kumbar VM, Peram MR, Patil S, Bhat KG, Diwan PV. Effect of resveratrol on biofilm formation and virulence factor gene expression of Porphyromonas gingivalis in periodontal disease. Apmis. 2019;127(4):187–95. https://doi.org/10.1111/apm.12930.

    Article  PubMed  Google Scholar 

  21. Jin Y, Samaranayake LP, Samaranayake Y, Yip HK. Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars. Arch Oral Biol. 2004;49(10):789–98. https://doi.org/10.1016/j.archoralbio.2004.04.011.

    Article  PubMed  Google Scholar 

  22. Sandasi M, Leonard CM, Viljoen AM. The in vitro antibiofilm activity of selected culinary herbs and medicinal plants against Listeria monocytogenes. Lett Appl Microbiol. 2010;50(1):30–5. https://doi.org/10.1111/j.1472-765X.2009.02747.x.

    Article  PubMed  Google Scholar 

  23. Shukla SK, Rao TS. An improved crystal violet assay for biofilm quantification in 96-well microtitre plate. BioRxiv. 2017. https://doi.org/10.1101/100214.

    Article  Google Scholar 

  24. Jaiswal S, Mishra P. Antimicrobial and antibiofilm activity of curcumin-silver nanoparticles with improved stability and selective toxicity to bacteria over mammalian cells. Med Microbiol Immunol. 2018;207(1):39–533. https://doi.org/10.1007/s00430-017-0525-y.

    Article  PubMed  Google Scholar 

  25. Grenier D, Morin MP, Fournier Larente J, Chen H. Vitamin D inhibits the growth of and virulence factor gene expression by Porphyromonas gingivalis and blocks activation of the nuclear factor kappa B transcription factor in monocytes. J Periodontal Res. 2016;51(3):359–65. https://doi.org/10.1111/jre.12315.

    Article  PubMed  Google Scholar 

  26. Shah T, Joshi K, Mishra S, Otiv S, Kumbar V. Molecular and cellular effects of vitamin B12 forms on human trophoblast cells in presence of excessive folate. Biomed Pharmacother. 2016;84:526–34. https://doi.org/10.1016/j.biopha.2016.09.071.

    Article  PubMed  Google Scholar 

  27. Cowan MM. Plant products as antimicrobial agents. Clin Microbiol Rev. 1999;12(4):564–82. https://doi.org/10.1128/CMR.12.4.564.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Bush K. Antibacterial drug discovery in the 21st century. Clin Microbiol Infect. 2004;10(54):10–7. https://doi.org/10.1111/j.1465-0691.2004.1005.x.

    Article  PubMed  Google Scholar 

  29. Kala BS, Gunjan C, Disha N, Shobha P. Treatment of periodontal disease-a herbal approach. Int J Pharm Sci Rev Res. 2015;33(2):126–36.

    Google Scholar 

  30. Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8(9):881–90. https://doi.org/10.3201/eid0809.020063.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Joo HS, Otto M. Molecular basis of in vivo biofilm formation by bacterial pathogens. Chem Biol. 2012;19(12):1503–13. https://doi.org/10.1016/j.chembiol.2012.10.022.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Grenier D, Chen H, Lagha AB, Fournier-Larente J, Morin MP. Dual action of myricetin on Porphyromonas gingivalis and the inflammatory response of host cells: a promising therapeutic molecule for periodontal diseases. PLoS ONE. 2015;10(6):e0131758. https://doi.org/10.1371/journal.pone.0131758.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Bao K, Belibasakis GN, Thurnheer T, Aduse-Opoku J, Curtis MA, Bostanci N. Role of Porphyromonas gingivalis gingipains in multi-species biofilm formation. BMC Microbiol. 2014;14:258. https://doi.org/10.1186/s12866-014-0258-7.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kariu T, Nakao R, Ikeda T, Nakashima K, Potempa J, Imamura T. Inhibition of gingipains and Porphyromonas gingivalis growth and biofilm formation by prenyl flavonoids. J Periodontal Res. 2017;52(1):89–96. https://doi.org/10.1111/jre.12372.

    Article  PubMed  Google Scholar 

  35. Moran JM, Rodriguez-Velasco FJ, Roncero-Martin R, Vera V, Pedrera-Zamorano JD. Cytotoxic effects of curcumin in osteosarcoma cells. Int J Nanomed. 2014;9:5273–5. https://doi.org/10.2147/IJN.S75005.

    Article  Google Scholar 

  36. Kriebel K, Hieke C, Müller-Hilke B, Nakata M, Kreikemeyer B. Oral biofilms from symbiotic to pathogenic interactions and associated disease-connection of periodontitis and rheumatic arthritis by peptidylarginine deiminase. Front Microbiol. 2018;9:53. https://doi.org/10.3389/fmicb.2018.00053.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Authors would like to thank Kancor Ingredients Ltd., India for supplying Curcumin as a gift sample.

Funding

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kishore G. Bhat.

Ethics declarations

Conflict of interest

The authors declare that there are no conflicts of interest in this study.

Ethical approval

The study was approved by the Institutional Review Board (Certificate No. 1810).

Informed consent

All authors read and agreed to the final manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumbar, V.M., Peram, M.R., Kugaji, M.S. et al. Effect of curcumin on growth, biofilm formation and virulence factor gene expression of Porphyromonas gingivalis. Odontology 109, 18–28 (2021). https://doi.org/10.1007/s10266-020-00514-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10266-020-00514-y

Keywords

Navigation