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Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 39, 2023 - Issue 6
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Research Article

Inhibitory effects of vorinostat (SAHA) against food-borne pathogen Salmonella enterica serotype Kentucky mixed culture biofilm with virulence and quorum-sensing relative expression

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Pages 617-628 | Received 21 Dec 2022, Accepted 24 Jul 2023, Published online: 14 Aug 2023

References

  • Ashrafudoulla M, Na KW, Byun KH, Kim DH, Yoon JW, Mizan MFR, Kang I, Ha SD. 2021. Isolation and characterization of Salmonella spp. from food and food contact surfaces in a chicken processing factory. Poult Sci. 100:101234. doi: 10.1016/j.psj.2021.101234.
  • Aswathanarayan JB, Vittal RR. 2018. Inhibition of biofilm formation and quorum sensing mediated phenotypes by berberine in Pseudomonas aeruginosa and Salmonella Typhimurium. RSC Adv. 8:36133–36141. doi: 10.1039/c8ra06413j.
  • Bajaj V, Hwang C, Lee CA. 1995. hilA is a novel ompR/toxR family member that activates the expression of Salmonella Typhimurium invasion genes. Mol Microbiol. 18:715–727. doi: 10.1111/j.1365-2958.1995.mmi_18040715.x.
  • Braga PC, Sasso MD, Sala MT. 2000. Sub-MIC concentrations of cefodizime interfere with various factors affecting bacterial virulence. J Antimicrob Chemother. 45:15–25. doi: 10.1093/jac/45.1.15.
  • Bridier A, Dubois-Brissonnet F, Boubetra A, Thomas V, Briandet R. 2010. The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J Microbiol Methods. 82:64–70. doi: 10.1016/j.mimet.2010.04.006.
  • Byun KH, Han SH, Yoon JW, Park SH, Ha SD. 2021. Efficacy of chlorine-based disinfectants (sodium hypochlorite and chlorine dioxide) on Salmonella Enteritidis planktonic cells, biofilms on food contact surfaces and chicken skin. Food Control. 123:107838. doi: 10.1016/j.foodcont.2020.107838.
  • Cacabelos R, Teijido O. 2018. Epigenetic drug discovery for Alzheimer’s disease. In: Moskalev A, Vaiserman AM, editors. Epigenetics of aging and longevity. Vol. 4. Cambridge (MA): Elsevier Inc.; p. 453–495.
  • CDC. 2021. https://www.cdc.gov/salmonella. /index.html.
  • Dantas STA, Rossi BF, Bonsaglia ECR, Castilho IG, Hernandes RT, Fernandes A, Rall VLM. 2018. Cross-contamination and biofilm formation by Salmonella enterica serovar Enteritidis on various cutting boards. Foodborne Pathog Dis. 15:81–85. doi: 10.1089/fpd.2017.2341.
  • DeFlorio W, Liu S, White AR, Taylor TM, Cisneros‐Zevallos L, Min Y, Scholar EM. 2021. Recent developments in antimicrobial and antifouling coatings to reduce or prevent contamination and cross‐contamination of food contact surfaces by bacteria. Compr Rev Food Sci Food Saf. 20:3093–3134. doi: 10.1111/1541-4337.12750.
  • Dewi G, Nair DVT, Peichel C, Johnson TJ, Noll S, Johny AK. 2021. Effect of lemongrass essential oil against multidrug-resistant Salmonella Heidelberg and its attachment to chicken skin and meat. Poult Sci. 100:101116. doi: 10.1016/j.psj.2021.101116.
  • Gambino M, Cappitelli F. 2016. Mini-review: biofilm responses to oxidative stress. Biofouling. 32:167–178. doi: 10.1080/08927014.2015.1134515.
  • Gao MJ, Chen GG, Wang HC, Xie BQ, Hu LN, Kong YY, Yang G, Tao Y, Han Y, Wu XS, et al. 2016. Therapeutic potential and functional interaction of carfilzomib and vorinostat in T-cell leukemia/lymphoma. Oncotarget. 7:29102–29115. doi: 10.18632/oncotarget.8667.
  • Gonzalez JE, Keshavan ND. 2006. Messing with bacterial quorum sensing. Microbiol Mol Biol Rev. 70:859–875. doi: 10.1128/MMBR.00002-06.
  • Ha DG, Kuchma SL, O'Toole GA. 2014. Plate-based assay for swimming motility in Pseudomonas aeruginosa. Methods Mol Biol. 1149:59–65. doi: 10.1007/978-1-4939-0473-0_7.
  • Hossain MI, Kim K, Mizan MFR, Toushik SH, Ashrafudoulla M, Roy PK, Nahar S, Jahid IK, Choi C, Park SH, et al. 2021. Comprehensive molecular, probiotic, and quorum-sensing characterization of anti-listerial lactic acid bacteria, and application as bioprotective in a food (milk) model. J Dairy Sci. 104:6516–6534. doi: 10.3168/jds.2020-19034.
  • Hossain MI, Mizan MFR, Ashrafudoulla M, Nahar S, Joo H-J, Jahid IK, Park SH, Kim K-S, Ha S-D. 2020. Inhibitory effects of probiotic potential lactic acid bacteria isolated from kimchi against Listeria monocytogenes biofilm on lettuce, stainless-steel surfaces, and MBEC™ biofilm device. LWT. 118:108864. doi: 10.1016/j.lwt.2019.108864.
  • Hossain MI, Mizan MFR, Roy PK, Nahar S, Toushik SH, Ashrafudoulla M, Jahid IK, Lee J, Ha S-D. 2021. Listeria monocytogenes biofilm inhibition on food contact surfaces by application of postbiotics from Lactobacillus curvatus B. 67 and Lactobacillus plantarum M. Food Res Int. 148:110595. doi: 10.1016/j.foodres.2021.110595.
  • Jeong J, Chon JW, Kim H, Song KY, Seo KH. 2018. Risk assessment for salmonellosis in chicken in South Korea: the effect of Salmonella concentration in chicken at retail. Korean J Food Sci Anim Resour. 38:1043–1054. doi: 10.5851/kosfa.2018.e37.
  • Joo HJ, Mizan MFR, Hossain MI, Lee DU, Ha SD. 2020. Enhanced elimination of Salmonella Typhimurium and Campylobacter jejuni on chicken skin by sequential exposure to ultrasound and peroxyacetic acid. J Food Saf. 40:e12803. doi: 10.1111/jfs.12803.
  • Kim YK, Roy PK, Ashrafudoulla M, Nahar S, Toushik SH, Hossain MI, Mizan MFR, Park SH, Ha S-D. 2022. Antibiofilm effects of quercetin against Salmonella enterica biofilm formation and virulence, stress response, and quorum-sensing gene expression. Food Control. 137:108964. doi: 10.1016/j.foodcont.2022.108964.
  • Lamoth F, Juvvadi PR, Steinbach WJ. 2015. Histone deacetylase inhibition as an alternative strategy against invasive aspergillosis. Front Microbiol. 6:96. doi: 10.3389/fmicb.2015.00096.
  • Lee KH, Lee JY, Roy PK, Mizan MFR, Hossain MI, Park SH, Ha SD. 2020. Viability of Salmonella Typhimurium biofilms on major food-contact surfaces and eggshell treated during 35 days with and without water storage at room temperature. Poult Sci. 99:4558–4565. doi: 10.1016/j.psj.2020.05.055.
  • Li X, Wu B, Chen H, Nan KH, Jin YY, Sun L, Wang BL. 2018. Recent developments in smart antibacterial surfaces to inhibit biofilm formation and bacterial infections. J Mater Chem B. 6:4274–4292. doi: 10.1039/c8tb01245h.
  • Liu XY, Lu R, Xia YL, Wu SP, Sun J. 2010. Eukaryotic signaling pathways targeted by Salmonella effector protein AvrA in intestinal infection in vivo. BMC Microbiol. 10:326. doi: 10.1186/1471-2180-10-326.
  • Martins ML, Pinto UM, Riedel K, Vanetti MCD. 2018. Quorum sensing and spoilage potential of Psychrotrophic Enterobacteriaceae isolated from milk. Biomed Res Int. 2018:2723157. doi: 10.1155/2018/2723157.
  • Mizan MFR, Jahid IK, Kim M, Lee KH, Kim TJ, Ha SD. 2016. Variability in biofilm formation correlates with hydrophobicity and quorum sensing among Vibrio parahaemolyticus isolates from food contact surfaces and the distribution of the genes involved in biofilm formation. Biofouling. 32:497–509. doi: 10.1080/08927014.2016.1149571.
  • Murray TS, Ledizet M, Kazmierczak BI. 2010. Swarming motility, secretion of type 3 effectors and biofilm formation phenotypes exhibited within a large cohort of Pseudomonas aeruginosa clinical isolates. J Med Microbiol. 59:511–520. doi: 10.1099/jmm.0.017715-0.
  • Nagel GM, Bauermeister LJ, Bratcher CL, Singh M, McKee SR. 2013. Salmonella and Campylobacter reduction and quality characteristics of poultry carcasses treated with various antimicrobials in a post-chill immersion tank. Int J Food Microbiol. 165:281–286. doi: 10.1016/j.ijfoodmicro.2013.05.016.
  • Nahar S, Ha AJW, Byun KH, Hossain MI, Mizan MFR, Ha SD. 2021. Efficacy of flavourzyme against Salmonella Typhimurium, Escherichia coli, and Pseudomonas aeruginosa biofilms on food-contact surfaces. Int J Food Microbiol. 336:108897. doi: 10.1016/j.ijfoodmicro.2020.108897.
  • Nahar S, Mizan MFR, Ha AJ, Ha SD. 2018. Advances and future prospects of enzyme-based biofilm prevention approaches in the food industry. Compr Rev Food Sci Food Saf. 17:1484–1502. doi: 10.1111/1541-4337.12382.
  • Nickerson CA, Curtiss R. 1997. Role of sigma factor RpoS in initial stages of Salmonella Typhimurium infection. Infect Immun. 65:1814–1823. doi: 10.1128/iai.65.5.1814-1823.1997.
  • Ong KS, Mawang CI, Daniel-Jambun D, Lim YY, Lee SM. 2018. Current anti-biofilm strategies and potential of antioxidants in biofilm control. Expert Rev anti Infect Ther. 16:855–864. doi: 10.1080/14787210.2018.1535898.
  • Rosman CW, van Dijl JM, Sjollema J. 2022. Interactions between the foreign body reaction and Staphylococcus aureus biomaterial-associated infection. Winning strategies in the derby on biomaterial implant surfaces. Crit Rev Microbiol. 48:624–640. doi: 10.1080/1040841X.2021.2011132.
  • Roy PK, Ha AJ, Mizan MFR, Hossain MI, Ashrafudoulla M, Toushik SH, Nahar S, Kim YK, Ha SD. 2021. Effects of environmental conditions (temperature, pH, and glucose) on biofilm formation of Salmonella enterica serotype Kentucky and virulence gene expression. Poult Sci. 100:101209. doi: 10.1016/j.psj.2021.101209.
  • Roy PK, Kim SH, Jeon EB, Park EH, Park SY. 2023. Inhibition of Listeria monocytogenes cocktail culture biofilms on crab and shrimp coupons and the expression of biofilm-related genes. Antibiotics. 12:1008. doi: 10.3390/antibiotics12061008.
  • Roy PK, Qamar AY, Fang X, Hassan BMS, Cho J. 2020. Effects of cobalamin on meiotic resumption and developmental competence of growing porcine oocytes. Theriogenology. 154:24–30. doi: 10.1016/j.theriogenology.2020.05.011.
  • Roy PK, Qamar AY, Fang X, Kim G, Bang S, De Zoysa M, Shin ST, Cho J. 2021. Chitosan nanoparticles enhance developmental competence of in vitro-matured porcine oocytes. Reprod Domest Anim. 56:342–350. doi: 10.1111/rda.13871.
  • Roy PK, Song MG, Jeon EB, Kim SH, Park SY. 2022. Antibiofilm efficacy of quercetin against Vibrio parahaemolyticus biofilm on food-contact surfaces in the food industry. Microorganisms. 10:1902. doi: 10.3390/microorganisms10101902.
  • Roy PK, Song MG, Park SY. 2022. Impact of quercetin against Salmonella Typhimurium biofilm formation on food–contact surfaces and molecular mechanism pattern. Foods. 11:977. doi: 10.3390/foods11070977.
  • Roy PK, Song MG, Park SY. 2022. The inhibitory effect of quercetin on biofilm formation of Listeria monocytogenes mixed culture and repression of virulence. Antioxidants. 11:1733. doi: 10.3390/antiox11091733.
  • Salehi S, Howe K, Brooks J, Lawrence ML, Bailey RH, Karsi A. 2016. Identification of Salmonella enterica serovar Kentucky genes involved in attachment to chicken skin. BMC Microbiol. 16:168. doi: 10.1186/s12866-016-0781-9.
  • Sinde E, Carballo J. 2000. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiol. 17:439–447. doi: 10.1006/fmic.2000.0339.
  • Skandamis PN, Nychas GJE. 2012. Quorum Sensing in the Context of Food Microbiology. Appl Environ Microbiol. 78:5473–5482. doi: 10.1128/AEM.00468-12.
  • Stebe-Frick S, Ostaff MJ, Stange EF, Malek NP, Wehkamp J. 2018. Histone deacetylase-mediated regulation of the antimicrobial peptide hBD2 differs in intestinal cell lines and cultured tissue. Sci Rep. 8:12886. doi: 10.1038/s41598-018-31125-x.
  • Stepanovic S, Cirkovic I, Ranin L, Svabic-Vlahovic M. 2004. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol. 38:428–432. doi: 10.1111/j.1472-765X.2004.01513.x.
  • Suo YJ, Huang YY, Liu YH, Shi CL, Shi XM. 2012. The expression of superoxide dismutase (SOD) and a putative ABC transporter permease is inversely correlated during biofilm formation in Listeria monocytogenes 4b G. PLoS One. 7:e48467. doi: 10.1371/journal.pone.0048467.
  • Tauxe RV, Doyle MP, Kuchenmüller T, Schlundt J, Stein CE. 2010. Evolving public health approaches to the global challenge of foodborne infections. Int J Food Microbiol. 139:S16–S28. doi: 10.1016/j.ijfoodmicro.2009.10.014.
  • Toushik SH, Kim K, Ashrafudoulla M, Mizan MFR, Roy PK, Nahar S, Kim Y, Ha S-D. 2021. Korean kimchi-derived lactic acid bacteria inhibit foodborne pathogenic biofilm growth on seafood and food processing surface materials. Food Control. 129:108276. doi: 10.1016/j.foodcont.2021.108276.
  • Tu B, Yin GD, Li H. 2020. Synergistic effects of vorinostat (SAHA) and azoles against Aspergillus species and their biofilms. BMC Microbiol. 20:28. doi: 10.1186/s12866-020-1718-x.
  • Wang HH, Dong Y, Wang GY, Xu XL, Zhou GH. 2016. Effect of growth media on gene expression levels in Salmonella Typhimurium biofilm formed on stainless steel surface. Food Control. 59:546–552. doi: 10.1016/j.foodcont.2015.06.026.
  • Wang HH, Ye KP, Wei XR, Cao JX, Xu XL, Zhou GH. 2013. Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control. 33:378–384. doi: 10.1016/j.foodcont.2013.03.030.
  • Wang YP, Li L, Shen JZ, Yang FJ, Wu YN. 2009. Quinolone-resistance in Salmonella is associated with decreased mRNA expression of virulence genes invA and avrA, growth and intracellular invasion and survival. Vet Microbiol. 133:328–334. doi: 10.1016/j.vetmic.2008.07.012.
  • Waters CM, Bassler BL. 2005. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol. 21:319–346. doi: 10.1146/annurev.cellbio.21.012704.131001.
  • Wayne P. 2011. Clinical and laboratory standards institute. In: Lewis JS II, editor. Performance standards for antimicrobial susceptibility testing. Wayne (PA): Clinical and Laboratory Standards Institute; p. 42–45.
  • Xu JN, Sun JJ, Wang PC, Ma XC, Li S. 2018. Pendant HDAC inhibitor SAHA derivatised polymer as a novel prodrug micellar carrier for anticancer drugs. J Drug Target. 26:448–457. doi: 10.1080/1061186X.2017.1419355.
  • Yang XJ, Brisbin J, Yu H, Wang Q, Yin FG, Zhang YG, Sabour P, Sharif S, Gong J. 2014. Selected lactic acid-producing bacterial isolates with the capacity to reduce Salmonella translocation and virulence gene expression in chickens. PLoS One. 9:e93022. doi: 10.1371/journal.pone.0093022.
  • Zhao XH, Zhao FH, Wang J, Zhong NJ. 2017. Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Adv. 7:36670–36683. doi: 10.1039/C7RA02497E.

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