Limonene inhibits streptococcal biofilm formation by targeting surface-associated virulence factors

Journal of Medical Microbiology

Volumn 64, Issue 8, 2015, Pages 879-890

  Subramenium, Ganapathy Ashwinkumar ^a   Vijayakumar, Karuppiah ^a   Pandian, Shunmugiah Karutha ^a  

^a ALAGAPPA UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; COVR PROTEIN; LIMONENE; M PROTEIN; MGA PROTEIN; PROTEINASE; UNCLASSIFIED DRUG; VICR PROTEIN; VIRULENCE FACTOR; ADHESIN; CYCLOHEXENE DERIVATIVE; TERPENE;

ANTIBACTERIAL ACTIVITY; ANTIBIOFILM ACTIVITY; ARTICLE; ASSAY; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM ISOLATE; BIOFILM; CITRUS FRUIT; COLONY FORMATION; CONTROLLED STUDY; DISEASE PREDISPOSITION; DOWN REGULATION; DRUG EFFICACY; GENE EXPRESSION; MICROSCOPY; MINIMAL BIOFILM INHIBITORY CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; STREPTOCOCCUS; STREPTOCOCCUS MITIS; STREPTOCOCCUS MUTANS; STREPTOCOCCUS PYOGENES; SURFACE COATING ASSAY; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION PROFILING; HUMAN; PHYSIOLOGY;

ADHESINS, BACTERIAL; ANTI-BACTERIAL AGENTS; BIOFILMS; CYCLOHEXENES; GENE EXPRESSION PROFILING; HUMANS; STREPTOCOCCUS MITIS; STREPTOCOCCUS MUTANS; STREPTOCOCCUS PYOGENES; TERPENES; VIRULENCE FACTORS;

EID: 84940194766     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.000105     Document Type: Article

References (60)

1. Adukwu, E. C., Allen, S. C. & Phillips, C. A. (2012). The anti-biofilm activity of lemongrass (Cymbopogon flexuosus) and grapefruit (Citrus paradisi) essential oils against five strains of Staphylococcus aureus. J Appl Microbiol 113, 1217-1227.
2. Baldassarri, L., Creti, R., Recchia, S., Imperi, M., Facinelli, B., Giovanetti, E., Pataracchia, M., Alfarone, G. & Orefici, G. (2006). Therapeutic failures of antibiotics used to treat macrolide-susceptible Streptococcus pyogenes infections may be due to biofilm formation. J Clin Microbiol 44, 2721-2727
3. Ban, S. H., Kim, J. E., Pandit, S. & Jeon, J. G. (2012). Influences of Dryopteris crassirhizoma extract on the viability, growth and virulence properties of Streptococcus mutans. Molecules 17, 9231-9244.
4. Bandara, H. M. H. N., Lam, O. L. T., Watt, R. M., Jin, L. J. & Samaranayake, L. P. (2010). Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species. J Med Microbiol 59, 1225-1234.
5. Bisno, A. L. (1991). Group A streptococcal infections and acute rheumatic fever. N Engl J Med 325, 783-793.
6. Bjarnsholt, T. (2013). The role of bacterial biofilms in chronic infections. APMIS Suppl 121 (Suppl. 136), 1-51.
7. Brown, T. A., Jr, Ahn, S. J., Frank, R. N., Chen, Y. Y. M., Lemos, J. A. & Burne, R. A. (2005). A hypothetical protein of Streptococcus mutans is critical for biofilm formation. Infect Immun 73, 3147-3151.
8. Budzyńska, A., Wieckowska-Szakiel, M., Sadowska, B., Kalemba, D. & Rózalska, B. (2011). Antibiofilm activity of selected plant essential oils and their major components. Pol J Microbiol 60, 35-41
9. Chaturvedi, T. (2013). Allergy related to dental implant and its clinical significance. Clin Cosmet Investig Dent 5, 57-61.
10. Chee, H. Y., Kim, H. & Lee, M. H. (2009). In vitro antifungal activity of limonene against Trichophyton rubrum. Mycobiology 37, 243-246.
11. Chen, Y., Zeng, H., Tian, J., Ban, X., Ma, B. & Wang, Y. (2013). Antifungal mechanism of essential oil from Anethum graveolens seeds against Candida albicans. J Med Microbiol 62, 1175-1183.
12. Chen, Z., He, D., Deng, J., Zhu, J. & Mao, Q. (2015). Chemical composition and antibacterial activity of the essential oil from Agathis dammara (Lamb.) rich fresh leaves. Nat Prod Res 29 (in press)
13. Cho, K. H. & Caparon, M. G. (2005). Patterns of virulence gene expression differ between biofilm and tissue communities of Strep-tococcus pyogenes. Mol Microbiol 57, 1545-1556.
14. Collin, M. & Olsén, A. (2003). Extracellular enzymes with immunomodulating activities: variations on a theme in Streptococcus pyogenes. Infect Immun 71, 2983-2992.
15. Conley, J., Olson, M. E., Cook, L. S., Ceri, H., Phan, V. & Davies, H. D. (2003). Biofilm formation by group A streptococci: is there a relationship with treatment failure? J Clin Microbiol 41, 4043-4048
16. Courtney, H. S., Hasty, D. L. & Dale, J. B. (2006). Antiphagocytic mechanisms of Streptococcus pyogenes: binding of fibrinogen to Mrelated protein. Mol Microbiol 59, 936-947.
17. Crater, D. L., Dougherty, B. A. & van de Rijn, I. (1995). Molecular characterization of hasC from an operon required for hyaluronic acid synthesis in group A streptococci. Demonstration of UDP-glucose pyrophosphorylase activity. J Biol Chem 270, 28676-28680
18. Cunningham, M. W. (2000). Pathogenesis of group A streptococcal infections. Clin Microbiol Rev 13, 470-511.
19. D’Angelis, C. E. M., Leite, M. F., Sousa, J. P. B., Alonso, L., Polizello, A. C. M., Groppo, M., Jr, Aires, C. P., Bastos, J. K. & Spadaro, A. C. C. (2012). Inhibiting effect of Dorstenia asaroides extracts on cariogenic properties of Streptococcus mutans. Anaerobe 18, 31-36.
20. Dalton, T. L. & Scott, J. R. (2004). CovS inactivates CovR and is required for growth under conditions of general stress in Streptococcus pyogenes. J Bacteriol 186, 3928-3937
21. Dalton, T. L., Collins, J. T., Barnett, T. C. & Scott, J. R. (2006). RscA, a member of the MDR1 family of transporters, is repressed by CovR and required for growth of Streptococcus pyogenes under heat stress. J Bacteriol 188, 77-85.
22. Davies, D. (2003). Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2, 114-122
23. Doern, C. D., Roberts, A. L., Hong, W., Nelson, J., Lukomski, S., Swords, W. E. & Reid, S. D. (2009). Biofilm formation by group A Streptococcus: a role for the streptococcal regulator of virulence (Srv) and streptococcal cysteine protease (SpeB). Microbiology 155, 46-52.
24. Elson, C. E., Maltzman, T. H., Boston, J. L., Tanner, M. A. & Gould, M. N. (1988). Anticarcinogenic activity of d-limonene during the initiation and promotion/progression stages of DMBA-induced rat mammary carcinogenesis. Carcinogenesis 9, 331-332.
25. Fischetti, V. A. (1989). Streptococcal M protein: molecular design and biological behavior. Clin Microbiol Rev 2, 285-314.
26. Gowrishankar, S., Poornima, B. & Pandian, S. K. (2014). Inhibitory efficacy of cyclo(L-leucyl-L-prolyl) from mangrove rhizosphere bacterium-Bacillus amyloliquefaciens (MMS-50) toward cariogenic properties of Streptococcus mutans. Res Microbiol 165, 278-289.
27. Graham, M. R., Smoot, L. M., Migliaccio, C. A. L., Virtaneva, K., Sturdevant, D. E., Porcella, S. F., Federle, M. J., Adams, G. J., Scott, J. R. & Musser, J. M. (2002). Virulence control in group A Streptococcus by a two-component gene regulatory system: global expression profiling and in vivo infection modeling. Proc Natl Acad Sci U S A 99, 13855-13860.
28. Green, A. E., Rowlands, R. S., Cooper, R. A. & Maddocks, S. E. (2012). The effect of the flavonol morin on adhesion and aggregation of Streptococcus pyogenes. FEMS Microbiol Lett 333, 54-58.
29. Hasan, S., Danishuddin, M., Adil, M., Singh, K., Verma, P. K. & Khan, A. U. (2012). Efficacy of E. officinalis on the cariogenic properties of Streptococcus mutans: a novel and alternative approach to suppress quorum-sensing mechanism. PLoS One 7, e40319.
30. Hoffman, L. R., D’Argenio, D. A., MacCoss, M. J., Zhang, Z., Jones, R. A. & Miller, S. I. (2005). Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436, 1171-1175.
31. Hollands, A., Aziz, R. K., Kansal, R., Kotb, M., Nizet, V. & Walker, M. J. (2008). A naturally occurring mutation in ropB suppresses SpeB expression and reduces M1T1 group A streptococcal systemic virulence. PLoS One 3, e4102.
32. Hytonen, J., Haataja, S., Gerlach, D., Podbielski, A. & Finne, J. (2001). The SpeB virulence factor of Streptococcus pyogenes, a multifunctional secreted and cell surface molecule with strepadhesin, lamininbinding and cysteine protease activity. Mol Microbiol 39, 512-519.
33. Igimi, H., Hisatsugu, T. & Nishimura, M. (1976). The use of D-limonene preparation as a dissolving agent of gallstones. Am J Dig Dis 21, 926-939.
34. Jaroenkit, P., Matan, N. & Nisoa, M. (2011). In vitro and in vivo activity of citronella oil for the control of spoilage bacteria of semi dried round scad (Decapterus maruadsi). Int J Med Arom Plants 1, 234-239.
35. Jenkinson, H. F. & Lamont, R. J. (1997). Streptococcal adhesion and colonization. Crit Rev Oral Biol Med 8, 175-200.
36. Kansal, R. G., McGeer, A., Low, D. E., Norrby-Teglund, A. & Kotb, M. (2000). Inverse relation between disease severity and expression of the streptococcal cysteine protease, SpeB, among clonal M1T1 isolates recovered from invasive group A streptococcal infection cases. Infect Immun 68, 6362-6369.
37. Karwacki, M. T., Kadouri, D. E., Bendaoud, M., Izano, E. A., Sampathkumar, V., Inzana, T. J. & Kaplan, J. B. (2013). Antibiofilm activity of Actinobacillus pleuropneumoniae serotype 5 capsular polysaccharide. PLoS One 8, e63844.
38. Korithoski, B., Lévesque, C. M. & Cvitkovitch, D. G. (2007). Involvement of the detoxifying enzyme lactoylglutathione lyase in Streptococcus mutans aciduricity. J Bacteriol 189, 7586-7592
39. Limsuwan, S., Kayser, O. & Voravuthikunchai, S. P. (2012). Antibacterial activity of Rhodomyrtus tomentosa (Aiton) Hassk. leaf extract against clinical isolates of Streptococcus pyogenes. Evid Based Complement Alternat Med 2012, 697183.
40. Lynskey, N. N., Lawrenson, R. A. & Sriskandan, S. (2011). New understandings in Streptococcus pyogenes. Curr Opin Infect Dis 24, 196-202
41. Lyon, W. R., Madden, J. C., Levin, J. C., Stein, J. L. & Caparon, M. G. (2001). Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 42, 145-157.
42. Malke, H. & Ferretti, J. J. (2007). CodY-affected transcriptional gene expression of Streptococcus pyogenes during growth in human blood. J Med Microbiol 56, 707-714.
43. Matsui, R. & Cvitkovitch, D. (2010). Acid tolerance mechanisms utilized by Streptococcus mutans. Future Microbiol 5, 403-417.
44. Nithya, C., Devi, M. G. & Karutha Pandian, S. (2011). A novel compound from the marine bacterium Bacillus pumilus S6-15 inhibits biofilm formation in Gram-positive and Gram-negative species. Biofouling 27, 519-528.
45. Nithyanand, P., Thenmozhi, R., Rathna, J. & Pandian, S. K. (2010). Inhibition of Streptococcus pyogenes biofilm formation by coral-associated actinomycetes. Curr Microbiol 60, 454-460.
46. Patenge, N., Fiedler, T. & Kreikemeyer, B. (2013). Common regulators of virulence in streptococci. Curr Top Microbiol Immunol 368, 111-153.
47. Ribardo, D. A., Lambert, T. J. & McIver, K. S. (2004). Role of Streptococcus pyogenes two-component response regulators in the temporal control of Mga and the Mga-regulated virulence gene emm. Infect Immun 72, 3668-3673.
48. Roberts, S. A. & Scott, J. R. (2007). RivR and the small RNA RivX: the missing links between the CovR regulatory cascade and the Mga regulon. Mol Microbiol 66, 1506-1522.
49. Roberts, A. L., Connolly, K. L., Kirse, D. J., Evans, A. K., Poehling, K. A., Peters, T. R. & Reid, S. D. (2012). Detection of group A Streptococcus in tonsils from pediatric patients reveals high rate of asymptomatic streptococcal carriage. BMC Pediatr 12, 3
50. Schillaci, D., Arizza, V., Dayton, T., Camarda, L. & Di Stefano, V. (2008). In vitro anti-biofilm activity of Boswellia spp. oleogum resin essential oils. Lett Appl Microbiol 47, 433-438.
51. Schuster, J. J. & Markx, G. H. (2014). Biofilm architecture. In Productive Biofilms (Advances in Biochemical Engineering/Biotechnology vol. 146), pp. 77-96. Edited by K. Muffler & R. Ulber. Berlin: Springer.
52. Selim, S. A., Adam, M. E., Hassan, S. M. & Albalawi, A. R. (2014). Chemical composition, antimicrobial and antibiofilm activity of the essential oil and methanol extract of the Mediterranean cypress (Cupressus sempervirens L.). BMC Complement Altern Med 14, 179-186.
53. Senadheera, M. D., Guggenheim, B., Spatafora, G. A., Huang, Y. C. C., Choi, J., Hung, D. C., Treglown, J. S., Goodman, S. D., Ellen, R. P. & Cvitkovitch, D. G. (2005). A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 187, 4064-4076.
54. Singh, P., Shukla, R., Prakash, B., Kumar, A., Singh, S., Mishra, P. K. & Dubey, N. K. (2010). Chemical profile, antifungal, antiaflatoxigenic and antioxidant activity of Citrus maxima Burm. and Citrus sinensis (L.) Osbeck essential oils and their cyclic monoterpene, DL-limonene. Food Chem Toxicol 48, 1734-1740.
55. Stipp, R. N., Boisvert, H., Smith, D. J., Hofling, J. F., Duncan, M. J. & Mattos-Graner, R. O. (2013). CovR and VicRK regulate cell surface biogenesis genes required for biofilm formation in Streptococcus mutans. PLoS One 8, e58271.
56. Sun, J. (2007). D-Limonene: safety and clinical applications. Altern Med Rev 12, 259-264.
57. Thenmozhi, R., Nithyanand, P., Rathna, J. & Pandian, S. K. (2009). Antibiofilm activity of coral-associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57, 284-294.
58. Thenmozhi, R., Balaji, K., Kumar, R., Rao, T. S. & Pandian, S. K. (2011). Characterization of biofilms in different clinical M serotypes of Streptococcus pyogenes. J Basic Microbiol 51, 196-204.
59. Wilkins, J. S., Jr (2002). US Patent no. 6 420 435. Washington, DC: US Patent and Trademark Office.
60. Zutkis, A. A., Anbalagan, S., Chaussee, M. S. & Dmitriev, A. V. (2014). Inactivation of the Rgg2 transcriptional regulator ablates the virulence of Streptococcus pyogenes. PLoS One 9, e114784