Punicalagin inhibits Salmonella virulence factors and has anti-quorum-sensing potential

Applied and Environmental Microbiology

Volumn 80, Issue 19, 2014, Pages 6204-6211

[No Author Info available]

Author keywords

[No Author keywords available]

Indexed keywords

ASSAYS; GENE EXPRESSION; GENES; MICROWAVE INTEGRATED CIRCUITS; POLYMERASE CHAIN REACTION; TRANSCRIPTION;

ANTI-MICROBIAL ACTIVITY; BROTH MICRODILUTION METHOD; CHROMOBACTERIUM VIOLACEUM; FOOD-BORNE PATHOGENS; INHIBITION ASSAYS; REVERSE TRANSCRIPTION; SALMONELLA INFECTIONS; SALMONELLA STRAINS;

SALMONELLA;

ADHESION; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOASSAY; INHIBITION; PATHOGEN; PHENOLIC COMPOUND; SWARMING; SWIMMING; VIRULENCE;

SALMONELLA;

ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; INDOLE DERIVATIVE; PUNICALAGIN; TANNIN; VIOLACEIN; VIRULENCE FACTOR;

ANTAGONISTS AND INHIBITORS; BACTERIUM ADHERENCE; CHROMOBACTERIUM; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; MICROBIAL SENSITIVITY TEST; PATHOGENICITY; PHYSIOLOGY; QUORUM SENSING; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; VIRULENCE;

ANTI-BACTERIAL AGENTS; BACTERIAL ADHESION; BACTERIAL PROTEINS; CHROMOBACTERIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; HYDROLYZABLE TANNINS; INDOLES; MICROBIAL SENSITIVITY TESTS; QUORUM SENSING; SALMONELLA TYPHIMURIUM; VIRULENCE; VIRULENCE FACTORS;

EID: 84907031382     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01458-14     Document Type: Article

References (42)

1. Hohmann EL. 2001. Nontyphoidal salmonellosis. Clin. Infect. Dis. 32: 263-269. http://dx.doi.org/10.1086/318457.
2. Kaur J, Jain S. 2012. Role of antigens and virulence factors of Salmonella enterica serovar Typhi in its pathogenesis. Microbiol. Res. 167:199-210. http://dx.doi.org/10.1016/j.micres.2011.08.001.
3. Vernikos GS, Parkhill J. 2006. Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22:2196-2203. http://dx.doi.org/10 .1093/bioinformatics/btl369.
4. Osborne SE, Coombes BK. 2011. Transcriptional priming of Salmonella Pathogenicity Island-2 precedes cellular invasion. PLoS One 6(6):e21648. http://dx.doi.org/10.1371/journal.pone.0021648.
5. Qiu J, Zhang X, Luo M, Li H, Dong J, Wang J, Leng B, Wang X, Feng H, Ren W, Deng X. 2011. Subinhibitory concentrations of Perilla oil affect the expression of secreted virulence factor genes in Staphylococcus aureus. PLoS One 6(1):e16160. http://dx.doi.org/10.1371/journal.pone .0016160.
6. Turgis M, Han J, Caillet S, Lacroix M. 2009. Antimicrobial activity of mustard essential oil against Escherichia coli O157: H7 and Salmonella typhi. Food Control 20:1073-1079. http://dx.doi.org/10.1016/j.foodcont .2009.02.001.
7. Cowan MM. 1999. Plant products as antimicrobial agents. Clin. Microbiol. Rev. 12:564-582.
8. Jiang TY, Li MY. 2013. Quorum sensing inhibitors: a patent review. Expert Opin. Ther. Pat. 23:867-894. http://dx.doi.org/10.1517/13543776 .2013.779674.
9. Musthafa KS, Sahu SK, Ravi AV, Kathiresan K. 2013. Anti-quorum sensing potential of the mangrove Rhizophora annamalayana. World J. Microbiol. Biotechnol. 29:1851-1858. http://dx.doi.org/10.1007/s11274 -013-1347-8.
10. Tan LY, Yin W-F, Chan K-G. 2013. Piper nigrum, Piper betle and Gnetum gnemon-natural food sources with anti-quorum sensing properties. Sensors 13:3975-3985. http://dx.doi.org/10.3390/s130303975.
11. Koh KH, Tham F-Y. 2011. Screening of traditional Chinese medicinal plants for quorum-sensing inhibitors activity. J. Microbiol. Immun. Infect. 44:144-148. http://dx.doi.org/10.1016/j.jmii.2009.10.001.
12. Miguel MG, Neves MA, Antunes MD. 2010. Pomegranate (Punica granatum L.): a medicinal plant with myriad biological properties-a short review. J. Med. Plants Res. 4:2836-2847.
13. Kulkarni AP, Mahal HS, Kapoor S, Aradhya SM. 2007. In vitro studies on the binding, antioxidant, and cytotoxic actions of punicalagin. J. Agric. Food Chem. 55:1491-1500. http://dx.doi.org/10.1021/jf0626720.
14. Glazer I, Masaphy S, Marciano P, Bar-Ilan I, Holland D, Kerem Z, Amir R. 2012. Partial identification of antifungal compounds from Punica granatum peel extracts. J. Agric. Food Chem. 60:4841-4848. http://dx.doi .org/10.1021/jf300330y.
15. Aqil F, Munagala R, Vadhanam MV, Kausar N, Jeyabalan J, Schultz DJ, Gupta RC. 2012. Anti-proliferative activity and protection against oxidative DNA damage by punicalagin isolated from pomegranate husk. Food Res. Int. 49:345-353. http://dx.doi.org/10.1016/j.foodres.2012.07.059.
16. Larrosa M, Tomas-Barberan FA, Espin JC. 2006. The dietary hydrolysable tannin punicalagin releases ellagic acid that induces apoptosis in human colon adenocarcinoma Caco-2 cells by using the mitochondrial pathway. J. Nutr. Biochem. 17:611-625. http://dx.doi.org/10.1016/j.jnutbio .2005.09.004.
17. Lin LT, Chen TY, Lin SC, Chung CY, Lin TC, Wang GH, Anderson R, Lin CC, Richardson CD. 2013. Broad-spectrum antiviral activity of chebulagic acid and punicalagin against viruses that use glycosaminoglycans for entry. BMC Microbiol. 13:187. http://dx.doi.org/10.1186/1471-2180 -13-187.
18. Lee SI, Kim BS, Kim KS, Lee S, Shin KS, Lim JS. 2008. Immunesuppressive activity of punicalagin via inhibition of NFAT activation. Biochem. Biophys. Res. Commun. 371:799-803. http://dx.doi.org/10 .1016/j.bbrc.2008.04.150.
19. Taguri T, Tanaka T, Kouno I. 2004. Antimicrobial activity of 10 different plant polyphenols against bacteria causing food-borne disease. Biol. Pharm. Bull. 27:1965-1969. http://dx.doi.org/10.1248/bpb.27.1965.
20. Al-Zoreky NS. 2009. Antimicrobial activity of pomegranate (Punica granatum L.) fruit peels. Int. J. Food Microbiol. 134:244-248. http://dx .doi.org/10.1016/j.ijfoodmicro.2009.07.002.
21. Clinical and Laboratory Standards Institute. 2005. Performance standards for antimicrobial susceptibility testing; fifteenth informational supplement, CLSI/NCCLS document M100-S15. Clinical and Laboratory Standards Institute, Wayne, PA.
22. Qiu J, Wang D, Xiang H, Feng H, Jiang Y, Xia L, Dong J, Lu J, Yu L, Deng X. 2010. Subinhibitory concentrations of thymol reduce enterotoxins A and B and -hemolysin production in Staphylococcus aureus isolates. PLoS One 5(3):e9736. http://dx.doi.org/10.1371/journal.pone.0009736.
23. Clemmer KM, Bonomo RA, Rather PN. 2011. Genetic analysis of surface motility in Acinetobacter baumannii. Microbiology 157:2534-2544. http: //dx.doi.org/10.1099/mic.0.049791-0.
24. Taganna JC, Quanico JP, Perono RMG, Amor EC, Rivera WL. 2011. Tannin-rich fraction from Terminalia catappa inhibits quorum sensing (QS) in Chromobacterium violaceum and the QS-controlled biofilm maturation and LasA staphylolytic activity in Pseudomonas aeruginosa. J. Ethnopharmacol. 134:865-871. http://dx.doi.org/10.1016/j.jep.2011.01.028.
25. Choo J, Rukayadi Y, Hwang JK. 2006. Inhibition of bacterial quorum sensing by vanilla extract. Lett. Appl. Microbiol. 42:637-641. http://dx.doi .org/10.1111/j.1472-765X.2006.01928.x.
26. -δδCT method. Methods 25: 402-408. http://dx.doi.org/10.1006/meth.2001.1262.
27. Chow S, Gu K, Jiang L, Nassour A. 2011. Salicylic acid affects swimming, twitching and swarming motility in Pseudomonas aeruginosa, resulting in decreased biofilm formation. J. Exp. Microbiol. Immunol. 15:22-29.
28. Inamuco J, Veenendaal AK, Burt SA, Post JA, Tjeerdsma-van Bokhoven JL, Haagsman HP, Veldhuizen EJ. 2012. Sub-lethal levels of carvacrol reduce Salmonella Typhimurium motility and invasion of porcine epithelial cells. Vet. Microbiol. 157:200-207. http://dx.doi.org/10.1016/j.vetmic .2011.12.021.
29. Burt SA, van der Zee R, Koets AP, de Graaff AM, van Knapen F, Gaastra W, Haagsman HP, Veldhuizen EJ. 2007. Carvacrol induces heat shock protein 60 and inhibits synthesis of flagellin in Escherichia coli O157: H7. Appl. Environ. Microbiol. 73:4484-4490. http://dx.doi.org/10.1128 /AEM.00340-07.
30. Shah DH, Zhou X, Addwebi T, Davis MA, Orfe L, Call DR, Guard J, Besser TE. 2011. Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system. Microbiology 157: 1428-1445. http://dx.doi.org/10.1099/mic.0.044461-0.
31. Groisman EA, Ochman H. 1997. How Salmonella became a pathogen. Trends Microbiol. 5:343-349. http://dx.doi.org/10.1016/S0966 -842X(97)01099-8.
32. Upadhyaya I, Upadhyay A, Kollanoor-Johny A, Darre MJ, Venkitanarayanan K. 2013. Effect of plant derived antimicrobials on Salmonella enteritidis adhesion to and invasion of primary chicken oviduct epithelial cells in vitro and virulence gene expression. Int. J. Mol. Sci. 14:10608- 10625. http://dx.doi.org/10.3390/ijms140510608.
33. Smith-Palmer A, Stewart J, Fyfe L. 2004. Influence of subinhibitory concentrations of plant essential oils on the production of enterotoxins A and B and -toxin by Staphylococcus aureus. J. Med. Microbiol. 53:1023- 1027. http://dx.doi.org/10.1099/jmm.0.45567-0.
34. Hansen-Wester I, Hensel M. 2001. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3:549-559. http://dx .doi.org/10.1016/S1286-4579(01)01411-3.
35. Finch R, Pritchard D, Bycroft B, Williams P, Stewart G. 1998. Quorum sensing: a novel target for anti-infective therapy. J. Antimicrob. Chemother. 42:569-571. http://dx.doi.org/10.1093/jac/42.5.569.
36. Hentzer M, Givskov M. 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J. Clin. Invest. 112:1300-1307. http://dx.doi.org/10.1172/JCI20074.
37. Zhu H, Sun S. 2008. Inhibition of bacterial quorum sensing-regulated behaviors by Tremella fuciformis extract. Curr. Microbiol. 57:418-422. http://dx.doi.org/10.1007/s00284-008-9215-8.
38. Surette MG, Bassler BL. 1998. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl. Acad. Sci. U. S. A. 95:7046-7050. http://dx.doi.org/10.1073/pnas.95.12.7046.
39. Dyszel JL, Smith JN, Lucas DE, Soares JA, Swearingen MC, Vross MA, Young GM, Ahmer BM. 2010. Salmonella enterica serovar Typhimurium can detect acyl homoserine lactone production by Yersinia enterocolitica in mice. J. Bacteriol. 192:29-37. http://dx.doi.org/10.1128/JB.01139-09.
40. Bearson BL, Bearson SM. 2008. The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. Microb. Pathog. 44:271-278. http://dx.doi.org/10.1016/j.micpath.2007.10.001.
41. Walthers D, Carroll RK, Navarre WW, Libby SJ, Fang FC, Kenney LJ. 2007. The response regulator SsrB activates expression of diverse Salmonella pathogenicity island 2 promoters and counters silencing by the nucleoid- associated protein H-NS. Mol. Microbiol. 65:477-493. http://dx .doi.org/10.1111/j.1365-2958.2007.05800.x.
42. Weir EK, Martin LC, Poppe C, Coombes BK, Boerlin P. 2008. Subinhibitory concentrations of tetracycline affect virulence gene expression in a multi-resistant Salmonella enterica subsp. enterica serovar Typhimurium DT104. Microbes Infect. 10:901-907. http://dx.doi.org/10.1016/j.micinf .2008.05.005.