Inhibition of quorum-sensing-controlled virulence factors of Pseudomonas aeruginosa by Murraya koenigii essential oil: A study in a Caenorhabditis elegans infectious model

Journal of Medical Microbiology

Volumn 65, Issue 12, 2016, Pages 1528-1535

  Ganesh, P Sankar ^a   Rai, Ravishankar Vittal ^a  

^a UNIVERSITY OF MYSORE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; ELASTASE; ESSENTIAL OIL; LASA PROTEASE; MURRAYA KOENIGII EXTRACT; PROTEINASE; PYOCYANINE; UNCLASSIFIED DRUG; VIRULENCE FACTOR; BACTERIAL PROTEIN; VEGETABLE OIL;

ANTIQUORUM SENSING ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; CAENORHABDITIS ELEGANS; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; IN VIVO STUDY; MURRAYA KOENIGII; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; QUORUM SENSING; ANIMAL; BIOFILM; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; GENETICS; HUMAN; INDIA; METABOLISM; MICROBIOLOGY; MURRAYA; PSEUDOMONAS INFECTIONS;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; CAENORHABDITIS ELEGANS; DISEASE MODELS, ANIMAL; HUMANS; INDIA; MURRAYA; OILS, VOLATILE; PLANT OILS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; QUORUM SENSING; VIRULENCE FACTORS;

EID: 85007314123     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.000385     Document Type: Article

References (71)

1. Adonizio, A. L., Downum, K., Bennett, B. C. &Mathee, K. (2006). Anti-quorum sensing activity of medicinal plants in southern Florida. J Ethnopharmacol 105,427-435.
2. Adonizio, A., Kong, K. F. &Mathee, K. (2008a). Inhibition of quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa by South Florida plant extracts. Antimicrob Agents Chemother 52,198-203.
3. Adonizio, A., Leal, S. M., Ausubel, F. M. &Mathee, K. (2008b). Attenuation of Pseudomonas aeruginosa virulence by medicinal plants in a Caeno-rhabditis elegans model system. J Med Microbiol 57, 809-813.
4. Bai A. J. &Rai, V. R. (2014). Quorum sensing inhibitory and anti-biofilm activity of essential oils and their in vivo efficacy in food systems. Food Biotechnol 28,269-292.
5. Bassole, I. H. &Juliani, H. R. (2012). Essential oils in combination and their antimicrobial properties. Molecules 17, 3989-4006.
6. Bjarnsholt, T., Jensen, P. O., Rasmussen, T. B., Christophersen, L., Calum, H., Hentzer, M., Hougen, H. P., Rygaard, J., Moser, C. &other authors (2005). Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151, 3873-3880.
7. Brackman, G., Cos, P., Maes, L., Nelis, H. J. &Coenye, T. (2011). Quo­rum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother 55, 2655-2661.
8. Brenner, S. (1974). The genetic of Caenorhabditis elegans. Genetics 77, 71­94.
9. Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods - a review. Int J Food Microbiol 94,223-253.
10. Caballero, A. R., Moreau, J. M., Engel, L. S., Marquart, M. E., Hill, J. M. &O’Callaghan, R. J. (2001). Pseudomonas aeruginosa protease IV enzyme assays and comparison to other Pseudomonas proteases. Anal Biochem 290, 330-337.
11. Chang, C. Y., Krishnan, T., Wang, H., Chen, Y., Yin, W. F., Chong, Y. M., Tan, L. Y., Chong, T. M. &Chan, K. G. (2014). Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone synthase as druggable target. Sci Rep 4, 7245.
12. Chuang, L. Y., Guh, J. Y., Chao, L. K., Lu, Y. C., Hwang, J. Y., Yang, Y.L., Cheng, T.-H., Yang, W.-Y., Chuen, Y. J. &other authors (2012). Anti-proliferative effects of cinnamaldehyde on human hepatoma cell lines. Food Chem 133,1603-1610.
13. Crouch Brewer, S., Wunderink, R. G., Jones, C. B. &Leeper, K. V. (1996). Ventilator-associated pneumonia due to Pseudomonas aeruginosa. Chest 109,1019-1029.
14. Darby, C., Cosma, C. L., Thomas, J. H. &Manoil, C. (1999). Lethal paral­ysis of Caenorhabditis elegans by Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96, 15202-15207.
15. De Kievit, T. R., Gillis, R., Marx, S., Brown, C. &Iglewski, B. H. (2001). Quorum-sensing genes in Pseudomonas aeruginosa biofilms: their role and expression patterns. Appl Environ Microbiol 67, 1865-1873.
16. Essar, D. W., Eberly, L., Hadero, A. &Crawford, I. P. (1990). Identifica­tion and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate syn-thases and evolutionary implications. J Bacteriol 172, 884-900.
17. Fuqua, C. &Greenberg, E. P. (1998). Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr Opin Microbiol 1, 183-189.
18. Gallagher, L. A. &Manoil, C. (2001). Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183, 6207-6214.
19. Gambello, M. J. &Iglewski, B. H. (1991). Cloning and characterization of the Pseudomonas aeruginosa lasR gene, a transcriptional activator of elastase expression. J Bacteriol 173, 3000-3009.
20. 2method against Pseudomonas aeruginosa. J Essent Oil Bear Pl 18, 264-275.
21. 2 method against Pseudomonas aeruginosa PAO1. Nat Prod Res 29, 2295-2298.
22. Gilabert, M., Ramos, A. N., Schiavone, M. M., Arena, M. E. &Bardon, A.(2011). Bioactive sesqui- and diterpenoids from the Argentine liverwort Porella chilensis. J Nat Prod 74, 574-579.
23. Gogoi, M., Sharma, A. &Hazarika, N. K. (2015). Biofilm formation by bacterial isolates from patients on indwelling medical devices. Indian JMed Microbiol 33,319-320.
24. Gooderham, W. J. &Hancock, R. E. (2009). Regulation ofvirulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 33, 279-294.
25. Haiyan, G., Lijuan, H., Shaoyu, L. &Ashraf, M. A. (2016). Antimicrobial, antibiofilm and antitumor activities of essential oil of Agastache rugosa from Xinjiang, China. Saudi JBiol Sci 23, 524-530.
26. Hancock, R. E. &Speert, D. P. (2000). Antibiotic resistance in Pseudomo-nas aeruginosa: mechanisms and impact on treatment. DrugResist Updat 3, 247-255.
27. Harjai, K., Gupta, R. K. &Sehgal, H. (2014). Attenuation of quorum sens­ing controlled virulence of Pseudomonas aeruginosa by cranberry. Indian J Med Res 139, 446-453.
28. Hoge, R., Pelzer, A., Rosenau, F. &Wilhelm, S. (2010). Weapons of apathogen: proteases and their role in virulence of Pseudomonas aeruginosa. In Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, number 2, pp. 383-395. Edited by A. Mendez-Vilas. Microbiology book series, Formatex Research Center.
29. Hopkins, R. S., Abbott, D. O. &Wallace, L. E. (1981). Follicular dermati­tis outbreak caused by Pseudomonas aeruginosa associated with a motel's indoor swimming pool. Public Health Rep 96, 246-249.
30. Husain, F. M., Ahmad, I., Khan, M. S., Ahmad, E., Tahseen, Q., Khan, M. S. &Alshabib, N. A. (2015). Sub-MICsof Mentha piperita essential oil and menthol inhibits AHL mediated quorum sensing and biofilm of Gram-negative bacteria. Front Microbiol 6, 420.
31. Jaramillo-Colorado, B., Olivero-Verbel, J., Stashenko, E. E., Wagner-Dobler, I. &Kunze, B. (2012). Anti-quorum sensing activity of essential oils from Colombian plants. Nat Prod Res 26, 1075-1086.
32. Kessler, E., Safrin, M., Olson, J. C. &Ohman, D. E. (1993). Secreted LasA of Pseudomonas aeruginosa is a staphylolytic protease. J Biol Chem 268, 7503-7508.
33. Khan, M. S. A., Zahin, M., Hasan, S., Husain, F. M. &Ahmad, I. (2009). Inhibition of quorum sensing regulated bacterial functions by plant essential oils with special reference to clove oil. Lett Appl Microbiol 49, 354-360.
34. Kim, Y. G., Lee, J. H., Kim, S. I., Baek, K. H. &Lee, J. (2015). Cinnamon bark oil and its components inhibit biofilm formation and toxin production. Int J Food Microbiol 195, 30-39.
35. Le Berre, R., Nguyen, S., Nowak, E., Kipnis, E., Pierre, M., Ader, F., Courcol, R., Guery, B. P., Faure, K. &Group, P. &Pyopneumagen Group. (2008). Quorum-sensing activity and related virulence factor expression in clinically pathogenic isolates of Pseudomonas aeruginosa. Clin Microbiol Infect 14, 337-343.
36. Liang, H., Duan, J., Sibley, C. D., Surette, M. G. &Duan, K. (2011). Iden­tification of mutants with altered phenazine production in Pseudomonas aeruginosa. JMed Microbiol 60, 22-34.
37. Lister, P. D., Wolter, D. J. &Hanson, N. D. (2009). Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chro-mosomally encoded resistance mechanisms. Clin Microbiol Rev 22, 582-610.
38. Liu, P. V. (1974). Extracellular toxins of Pseudomonas aeruginosa. J Infect Dis 130, S94-S99.
39. Mahajan-Miklos, S., Tan, M. W., Rahme, L. G. &Ausubel, F. M. (1999). Molecular mechanisms of bacterial virulence elucidated using a Pseudomo-nas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 47-56.
40. Mandal, S., Nayak, A., Kar, M., Banerjee, S. K., Das, A., Upadhyay, S. N., Singh, R. K., Banerji, A. &Banerji, J. (2010). Antidiar-rhoeal activity of carbazole alkaloids from Murraya koenigii Spreng (Ruta-ceae) seeds. Fitoterapia 81, 72-74.
41. Manefield, M., de Nys, R., Kumar, N., Read, R., Givskov, M., Steinberg, P. &Kjelleberg, S. (1999). Evidence that halogenated fura-nones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology 145, 283-291.
42. Mendelson, M. H., Gurtman, A., Szabo, S., Neibart, E., Meyers, B. R., Policar, M., Cheung, T. W., Lillienfeld, D., Hammer, G. & other authors (1994). Pseudomonas aeruginosa bacteremia in patients with AIDS. Clin Infect Dis 18, 886-895.
43. Nagappan, T., Segaran, T. C., Wahid, M. E., Ramasamy, P. &Vairappan, C. S. (2012). Efficacy of carbazole alkaloids, essential oil and extract of Murraya koenigii in enhancing subcutaneous wound healing in rats. Molecules 17, 14449-14463.
44. Nicas, T. I. &Iglewski, B. H. (1985). The contribution of exoproducts to virulence of Pseudomonas aeruginosa. Can J Microbiol 31, 387-392.
45. Noolu, B., Ajumeera, R., Chauhan, A., Nagalla, B., Manchala, R. &Ismail, A. (2013). Murraya koenigii leaf extract inhibits proteasome activity and induces cell death in breast cancer cells. BMC Complement Altern Med 13, 7.
46. Ochsner, U. A. &Reiser, J. (1995). Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92, 6424-6428.
47. Orhan, I. E., Mesaik, M. A., Jabeen, A. &Kan, Y. (2016). Immunomodula-tory properties of various natural compounds and essential oils through modulation of human cellular immune response. Ind Crops Prod 81, 117-122.
48. Pai, S., Bedford, L., Ruramayi, R., Aliyu, S. H., Sule, J., Maslin, D. &Enoch, D. A. (2016). Pseudomonas aeruginosa eningitis/ventriculitis in a UK tertiary referral hospital. QJM 109, 85-89.
49. Pearson, J. P., Gray, K. M., Passador, L., Tucker, K. D., Eberhard, A., Iglewski, B. H. &Greenberg, E. P. (1994). Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc NatlAcadSci USA 91, 197-201.
50. Pearson, J. P., Passador, L., Iglewski, B. H. &Greenberg, E. P. (1995). A second N-acylhomoserine lactone signal produced by Pseudomonas aeru-ginosa. Proc Natl Acad Sci USA 92, 1490-1494.
51. Pearson, J. P., Pesci, E. C. &Iglewski, B. H. (1997). Roles of Pseudomo-nas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179, 5756-5767.
52. Pessi, G. &Haas, D. (2000). Transcriptional control of the hydrogen cyanide biosynthetic genes hcnABC by the anaerobic regulator ANR and the quorum-sensing regulators LasR and RhlR in Pseudomonas aerugi-nosa. J Bacteriol 182, 6940-6949.
53. Rasmussen, T. B., Bjarnsholt, T., Skindersoe, M. E., Hentzer, M., Kristoffersen, P., Kote, M., Nielsen, J., Eberl, L. &Givskov, M. (2005). Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 187, 1799-1814.
54. Sasidharan, I. &Menon, A. N. (2011). Effects of temperature and solvent on antioxidant properties of curry leaf (Murraya koenigii L.). J Food Sci Technol 48,366-370.
55. Schmelzer, G. H. &Gurib-Fakim, A. (2013). Plant resources of tropical Africa 11(2). Medicianl plants 2. PROTA Foundation, Wageningen, Neth-erlands/CTA, Wageningen, Netherlands. 384.
56. Sepahi, E., Tarighi, S., Ahmadi, F. S. &Bagheri, A. (2015). Inhibition of quorum sensing in Pseudomonas aeruginosa by two herbal essential oils from Apiaceae family. J Microbiol 53, 176-180.
57. Shah, P., Singh, S. P. &Kumar, A. (2015). Combined effect of hydroetha-nolic extracts of Murraya koenigii and Phyllanthus niruri leaves on paracetamol and ethanol-induced toxicity in HepG2 cell line. CurrSci 109,1320-1326.
58. Shigemura, K., Arakawa, S., Sakai, Y., Kinoshita, S., Tanaka, K. &Fujisawa, M. (2006). Complicated urinary tract infection caused by Pseudomonas aeruginosa in a single institution (1999-2003). Int J Urol 13, 538-542.
59. Singh, B. N., Singh, H. B., Singh, A., Singh, B. R., Mishra, A. &Nautiyal, C. S. (2012). Lagerstroemia speciosa fruit extract modulates quorum sensing-controlled virulence factor production and biofilm formation in Pseudomonas aeruginosa. Microbiology 158, 529-538.
60. Spencer, R. C. (1996). Predominant pathogens found in the European Prevalence of Infection in Intensive Care Study. Eur J Clin Microbiol Infect Dis 15,281-285.
61. Steinstraesser, L., Tack, B. F., Waring, A. J., Hong, T., Boo, L. M., Fan, M. H., Remick, D. I., Su, G. L., Lehrer, R. I. &Wang, S. C. (2002). Activity of novispirin G10 against Pseudomonas aeruginosa in vitro and in infected burns. Antimicrob Agents Chemother 46, 1837-1844.
62. Stiernagle, T. (1999). Maintenance of C. elegans. In C. elegans a Practical Approach, pp. 51-67. Edited byA. HopeI. Oxford: Oxford UniversityPress.
63. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., Brinkman, F. S., Hufnagle, W. O., Kowalik, D. J. &other authors (2000). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964.
64. Tan, L. Y., Yin, W. F. &Chan, K. G. (2012). Silencing quorum sensing through extracts of Melicope lunu-ankenda. Sensors 12, 4339-4351.
65. Teplitski, M., Robinson, J. B. &Bauer, W. D. (2000). Plants secrete sub­stances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13, 637-648.
66. Treangen, T. J., Maybank, R. A., Enke, S., Friss, M. B., Diviak, L. F., Karaolis, D. K. R., Koren, S., Ondov, B., Phillippy, A. M. &otherauthors (2014). Complete genome sequence of the quality control strain Staphylococcus aureus subsp. aureus ATCC 25923. Genome Announc 2, e01110-e01114.
67. Van Delden, C. &Iglewski, B. H. (1998). Cell-to-cell signaling and Pseudomonasaeruginosa infections. Emerg Infect Dis 4, 551-560.
68. Vats, M., Singh, H. &Sardana, S. (2011). Phytochemical screening and antimicrobial activity of roots of Murraya koenigii (Linn.) Spreng. (Ruta-ceae). Braz J Microbiol 42, 1569-1573.
69. Vattem, D. A., Mihalik, K., Crixell, S. H. &McLean, R. J. C. (2007).Dietary phytochemicals as quorum sensing inhibitors. Fitoterapia 78, 302-310.
70. Yada, S., Vats, V., Dhunnoo, Y. &Gro, J. K. (2002). Hypoglycemic and antihyperglycemic activity of Murraya koenigii leaves in diabetic rats. J Ethnopharmacol 82, 111-116.
71. Zheng, S. Q., Ding, A. J., Li, G. P., Wu, G. S. &Luo, H. R. (2013). Drug absorption efficiency in Caenorhbditis elegans delivered by different methods. PLoS One 8, e56877-e56879