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http://dx.doi.org/10.4142/jvs.2018.19.6.808

Combination of berberine and ciprofloxacin reduces multi-resistant Salmonella strain biofilm formation by depressing mRNA expressions of luxS, rpoE, and ompR  

Shi, Chenxi (College of Veterinary Medicine, Northeast Agricultural University)
Li, Minmin (College of Veterinary Medicine, Northeast Agricultural University)
Muhammad, Ishfaq (College of Veterinary Medicine, Northeast Agricultural University)
Ma, Xin (Harbin Veterinary Research Institute of Chinese Academy of Agricultural Sciences)
Chang, Yicong (College of Veterinary Medicine, Northeast Agricultural University)
Li, Rui (College of Veterinary Medicine, Northeast Agricultural University)
Li, Changwen (Harbin Veterinary Research Institute of Chinese Academy of Agricultural Sciences)
He, Jingshan (College of Veterinary Medicine, Northeast Agricultural University)
Liu, Fangping (College of Veterinary Medicine, Northeast Agricultural University)
Publication Information
Journal of Veterinary Science / v.19, no.6, 2018 , pp. 808-816 More about this Journal
Abstract
Bacterial biofilms have been demonstrated to be closely related to clinical infections and contribute to drug resistance. Berberine, which is the main component of Coptis chinensis, has been reported to have efficient antibacterial activity. This study aimed to investigate the potential effect of a combination of berberine with ciprofloxacin (CIP) to inhibit Salmonella biofilm formation and its effect on expressions of related genes (rpoE, luxS, and ompR). The fractional inhibitory concentration (FIC) index of the combination of berberine with CIP is 0.75 showing a synergistic antibacterial effect. The biofilm's adhesion rate and growth curve showed that the multi-resistant Salmonella strain had the potential to form a biofilm relative to that of strain CVCC528, and the antibiofilm effects were in a dose-dependent manner. Biofilm microstructures were rarely observed at $1/2{\times}MIC/FIC$ concentrations (MIC, minimal inhibition concentration), and the combination had a stronger antibiofilm effect than each of the antimicrobial agents used alone at $1/4{\times}FIC$ concentration. LuxS, rpoE, and ompR mRNA expressions were significantly repressed (p< 0.01) at $1/2{\times}MIC/FIC$ concentrations, and the berberine and CIP combination repressed mRNA expressions more strongly at the $1/4{\times}FIC$ concentration. The results indicate that the combination of berberine and CIP has a synergistic effect and is effective in inhibiting Salmonella biofilm formation via repression of luxS, rpoE, and ompR mRNA expressions.
Keywords
Salmonella; berberine; biofilm; drug combinations; multidrug resistance;
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1 Ong ES, Woo SO, Yong YL. Pressurized liquid extraction of berberine and aristolochic acids in medicinal plants. J Chromatogr A 2000, 904, 57-64.   DOI
2 Rachid S, Ohlsen K, Witte W, Hacker J, Ziebuhr W. Effect of subinhibitory antibiotic concentrations on polysaccharide intercellular adhesin expression in biofilm-forming Staphylococcus epidermidis. Antimicrob Agents Chemother 2000, 44, 3357-3363.   DOI
3 Rao RS, Karthika RU, Singh SP, Shashikala P, Kanungo R, Jayachandran S, Prashanth K. Correlation between biofilm production and multiple drug resistance in imipenem resistant clinical isolates of Acinetobacter baumannii. Indian J Med Microbiol 2008, 26, 333-337.   DOI
4 Sela S, Frank S, Belausov E, Pinto R. A mutation in the luxS gene influences Listeria monocytogenes biofilm formation. Appl Environ Microbiol 2006, 72, 5653-5658.   DOI
5 Sharma M, Manoharlal R, Negi AS, Prasad R. Synergistic anticandidal activity of pure polyphenol curcumin I in combination with azoles and polyenes generates reactive oxygen species leading to apoptosis. FEMS Yeast Res 2010, 10, 570-578.
6 Steenackers HP, Janssens JC, Levin J, Voet A, De Maeyer M, De Vos DE, Vanderleyden J, De Keersmaecker SJ. Inhibition of salmonella biofilm formation: a sustainable alternative in the production of safe and healthy food. Commun Agric Appl Biol Sci 2008, 73, 71-76.
7 Castelijn GA, van der Veen S, Zwietering MH, Moezelaar R, Abee T. Diversity in biofilm formation and production of curli fimbriae and cellulose of Salmonella Typhimurium strains of different origin in high and low nutrient medium. Biofouling 2012, 28, 51-63.   DOI
8 Abdallah M, Benoliel C, Drider D, Dhulster P, Chihib NE. Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch Microbiol 2014, 196, 453-472.   DOI
9 Bai L, Zhao J, Gan X, Wang J, Zhang X, Cui S, Xia S, Hu Y, Yan S, Wang J, Li F, Fanning S, Xu J. Emergence and diversity of Salmonella enterica serovar Indiana isolates with concurrent resistance to ciprofloxacin and cefotaxime from patients and food-producing animals in China. Antimicrob Agents Chemother 2016, 60, 3365-3371.   DOI
10 Castelijn GA, Parabirsing JA, Zwietering MH, Moezelaar R, Abee T. Surface behaviour of S. Typhimurium, S. Derby, S. Brandenburg and S. Infantis. Vet Microbiol 2013, 161, 305-314.   DOI
11 Yang Y, Ye XL, Li XG, Zhen J, Zhang B, Yuan L. Synthesis and antimicrobial activity of 8-alkylberberine derivatives with a long aliphatic chain. Planta Med 2007, 73, 602-604.   DOI
12 Sun Y, Dai M, Hao H, Wang Y, Huang L, Almofti YA, Liu Z, Yuan Z. The role of RamA on the development of ciprofloxacin resistance in Salmonella enterica serovar Typhimurium. PLoS One 2011, 6, e23471.   DOI
13 Tobin DM, Vary JC Jr, Ray JP, Walsh GS, Dunstan SJ, Bang ND, Hagge DA, Khadge S, King MC, Hawn TR, Moens CB, Ramakrishnan L. The lta4h locus modulates susceptibility to mycobacterial infection in zebrafish and humans. Cell 2010, 140, 717-730.   DOI
14 Wang S, Yang Y, Zhao Y, Zhao H, Bai J, Chen J, Zhou Y, Wang C, Li Y. Sub-MIC tylosin inhibits Streptococcus suis biofilm formation and results in differential protein expression. Front Microbiol 2016, 7, 384.
15 Yang YB, Wang S, Wang C, Huang QY, Bai JW, Chen JQ, Chen XY, Li YH. Emodin affects biofilm formation and expression of virulence factors in Streptococcus suis ATCC700794. Arch Microbiol 2015, 197, 1173-1180.   DOI
16 Yu HH, Kim KJ, Cha JD, Kim HK, Lee YE, Choi NY, You YO. Antimicrobial activity of berberine alone and in combination with ampicillin or oxacillin against methicillinresistant Staphylococcus aureus. J Med Food 2005, 8, 454-461.   DOI
17 Choi JS, Ali MY, Jung HA, Oh SH, Choi RJ, Kim EJ. Protein tyrosine phosphatase 1B inhibitory activity of alkaloids from Rhizoma Coptidis and their molecular docking studies. J Ethnopharmacol 2015, 171, 28-36.   DOI
18 Zhao H, Zhou S, Zhang M, Feng J, Wang S, Wang D, Geng Y, Wang X. An in vitro AChE inhibition assay combined with UF-HPLC-ESI-Q-TOF/MS approach for screening and characterizing of AChE inhibitors from roots of Coptis chinensis Franch. J Pharm Biomed Anal 2016, 120, 235-240.   DOI
19 Zogaj X, Bokranz W, Nimtz M, Romling U. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect Immun 2003, 71, 4151-4158.   DOI
20 Chakraborty S, Mizusaki H, Kenney LJ. A FRET-based DNA biosensor tracks OmpR-dependent acidification of Salmonella during macrophage infection. PLoS Biol 2015, 13, e1002116.   DOI
21 Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI Supplement M100. CLSI, Wayne, 2018.
22 Cogan TA, Humphrey TJ. The rise and fall of Salmonella Enteritidis in the UK. J Appl Microbiol 2003, 94 Suppl, 114S-119S.   DOI
23 Dai C, Wang J, Kong W, Xiao X, Peng C, Zhao Y, Jin C. Investigation on the antibacterial activity of Coptis chinensis Franch and its components compatibility by microcalorimetry. Acta Chim Sinica 2010, 68, 936-940.
24 Garmendia J, Beuzon CR, Ruiz-Albert J, Holden DW. The roles of SsrA-SsrB and OmpR-EnvZ in the regulation of genes encoding the Salmonella typhimurium SPI-2 type III secretion system. Microbiology 2003, 149, 2385-2396.   DOI
25 Jeong HH, Jeong SG, Park A, Jang SC, Hong SG, Lee CS. Effect of temperature on biofilm formation by Antarctic marine bacteria in a microfluidic device. Anal Biochem 2014, 446, 90-95.   DOI
26 Kim JH, Yu D, Eom SH, Kim SH, Oh J, Jung WK, Kim YM. Synergistic antibacterial effects of chitosan-caffeic acid conjugate against antibiotic-resistant acne-related bacteria. Mar Drugs 2017, 15, 167.   DOI
27 Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the $2^{-{\Delta}{\Delta}CT}$ method. Methods 2001, 25, 402-408.   DOI
28 Li J, Overall CC, Nakayasu ES, Kidwai AS, Jones MB, Johnson RC, Nguyen NT, McDermott JE, Ansong C, Heffron F, Cambronne ED, Adkins JN. Analysis of the Salmonella regulatory network suggests involvement of SsrB and H-NS in ${\sigma}^{E}$-regulated SPI-2 gene expression. Front Microbiol 2015, 6, 27.
29 Li YH, Zhou YH, Ren YZ, Xu CG, Liu X, Liu B, Chen JQ, Ding WY, Zhao YL, Yang YB, Wang S, Liu D. Inhibition of Streptococcus suis adhesion and biofilm formation in vitro by water extracts of Rhizoma Coptidis. Front Pharmacol 2018, 9, 371.   DOI
30 Ling H, Kang A, Tan MH, Qi X, Chang MW. The absence of the luxS gene increases swimming motility and flagella synthesis in Escherichia coli K12. Biochem Biophys Res Commun 2010, 401, 521-526.   DOI
31 Marshall BM, Levy SB. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev 2011, 24, 718-733.   DOI
32 Norden CW, Wentzel H, Keleti E. Comparison of techniques for measurement of in vitro antibiotic synergism. J Infect Dis 1979, 140, 629-633.   DOI