Polyphenols as Inhibitors of Antibiotic Resistant Bacteria—Mechanisms Underlying Rutin Interference with Bacterial Virulence
Abstract
:1. Introduction
2. Results
2.1. Polyphenols Are Able to Inhibit Growth of Antibiotic Resistant Bacteria
2.2. Polyphenols Reduce the Ability of P. aeruginosa IBRS P001 to Form Biofilms
2.3. Polyphenols Are Mainly Non-Cytotoxic towards HaCaT Cells
2.4. Rutin Significantly Affected Urinary Catheter Biofilms
2.5. Co-Incubation with Rutin Reduced Bacterial Adhesion to HaCaT
2.6. Co-Incubation with Rutin Affects Different Aspects of Biofilm Formation
2.7. Rutin Can Eradicate Pre-Formed Biofilms by Diverse Mechanisms
2.8. Rutin Suppresses P. aeruginosa IBRS P001 Virulence Factors Production
2.9. Rutin Suppresses the P. aeruginosa IBRS P001 QS Systems Expression
2.10. Rutin’s Impact on Cell Membrane Permeability
3. Discussion
4. Materials and Methods
4.1. Antimicrobial Assay
4.2. Crystal Violet Antibiofilm Assay
4.3. Evaluation of Cytotoxicity in HaCaT Cell Line
4.4. Catheter Biofilm Inhibition/Eradication Model
4.5. P. aeruginosa and MRSA Adhesion to HaCaT Cells
4.6. Mechanisms of Rutin Biofilm Inhibition/Eradication
4.6.1. Biofilm MTT Assay
4.6.2. Congo Red Binding Assay
4.6.3. Quantification of eDNA
4.6.4. Rutin Biofilm Eradication Mechanisms
4.7. Extracellular Virulence Factors Analysis
4.7.1. Protease Assay
4.7.2. Elastase Assay
4.7.3. Pyocyanin Assay
4.7.4. Rhamnolipid Assay
4.8. RT-qPCR Analysis
4.9. Membrane Permeability Assay
4.10. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Bacteria | Hesperetin | Hesperidin | Naringenin | Naringin | Taxifolin | Rutin | Isoquercitrin | Morin | Chlorogenic Acid | Ferrulic Acid | p-Coumaric Acid | Gallic Acid | Streptomycin | |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Methicillin resistant S. aureus IBRS MRSA 011 | MIC | 0.5 | 0.5 | 0.25 | 0.5 | 0.25 | 0.5 | 0.5 | 0.12 | 0.5 | 0.5 | 0.5 | >1 | 0.1 |
MBC | 1 | 1 | 0.5 | 1 | 0.5 | 1 | 1 | 0.25 | 1 | 1 | 1 | >1 | 0.8 | |
P. aeruginosa IBRS P001 | MIC | 0.5 | 0.5 | 0.25 | 0.25 | 0.25 | 0.5 | 0.25 | 0.12 | 0.5 | 0.5 | 0.5 | >1 | 0.05 |
MBC | 1 | 1 | 0.5 | 0.5 | 0.5 | 1 | 0.5 | 0.25 | 1 | 1 | 1 | >1 | 0.1 | |
P. aeruginosa MMA83 | MIC | 1 | 1 | 1 | >1 | 1 | 0.5 | 0.25 | 1 | 1 | 1 | 0.5 | 1 | >1 |
MBC | 1 | 1 | 1 | >1 | >1 | 0.5 | 0.25 | 1 | >1 | 1 | 1 | 1 | >1 | |
E. coli IBRS E003 | MIC | >1 | >1 | 0.5 | >1 | 0.5 | >1 | >1 | 0.25 | >1 | >1 | >1 | >1 | 0.1 |
MBC | >1 | >1 | 1 | >1 | 1 | >1 | >1 | 0.5 | >1 | >1 | >1 | >1 | 0.2 | |
E. coli IMD989 | MIC | >1 | >1 | 1 | >1 | 1 | 1 | 1 | >1 | >1 | 1 | 1 | >1 | 1 |
MBC | >1 | >1 | >1 | >1 | 1 | 1 | 1 | >1 | >1 | 1 | 1 | >1 | >1 | |
A. baumannii 6077/12 | MIC | 0.5 | 0.5 | 0.5 | >1 | 0.5 | 0.5 | 0.25 | 0.5 | 1 | 0.5 | 0.5 | 0.5 | >1 |
MBC | 0.5 | 0.5 | 0.5 | >1 | 1 | 0.5 | 0.5 | 0.5 | 1 | 0.5 | 0.5 | 1 | >1 | |
A. baumannii S2/2 | MIC | 0.5 | 0.5 | 0.5 | >1 | 0.5 | 0.5 | 0.5 | 0.5 | 1 | 0.5 | 0.5 | 0.5 | >1 |
MBC | 0.5 | 0.5 | 0.5 | >1 | 0.5 | 0.5 | 0.5 | 0.5 | >1 | 0.5 | 0.5 | 0.5 | >1 | |
K. pneumoniae Ni9 | MIC | 1 | 1 | 0.25 | >1 | 1 | 1 | 0.5 | 0.5 | >1 | 1 | 1 | 1 | >1 |
MBC | 1 | 1 | 0.5 | >1 | 1 | 1 | 1 | 1 | >1 | 1 | 1 | 1 | >1 | |
K. pneumoniae IT977 | MIC | >1 | 1 | 1 | >1 | >1 | 1 | 1 | >1 | >1 | 1 | 1 | 1 | >1 |
MBC | >1 | 1 | 1 | >1 | >1 | 1 | 1 | >1 | >1 | 1 | 1 | 1 | >1 | |
A. xylosoxidans 37F | MIC | 1 | 1 | 1 | >1 | 1 | 0.5 | 0.5 | 0.5 | 1 | 1 | 1 | 0.5 | >1 |
MBC | 1 | 1 | 1 | >1 | 1 | 1 | 0.5 | 1 | >1 | 1 | 1 | 1 | >1 | |
S. infantis 1371/1 | MIC | >1 | >1 | >1 | >1 | >1 | 1 | 1 | >1 | >1 | 1 | 1 | >1 | >1 |
MBC | >1 | >1 | >1 | >1 | >1 | 1 | 1 | >1 | >1 | 1 | 1 | >1 | >1 |
Polyphenol | IC50 (mg/mL) |
---|---|
Hesperetin | >1 |
Hesperidin | >1 |
Naringenin | 0.528 ± 0.047 |
Naringin | >1 |
Taxifolin | 0.495 ± 0.047 |
Rutin | >1 |
Isoquercitrin | >1 |
Morin | 0.347 ± 0.016 |
Chlorogenic acid | 0.279 ± 0.008 |
Ferulic acid | >1 |
p-coumaric acid | >1 |
Gallic acid | <0.080 |
Strain | Resistance | Reference |
---|---|---|
Methicillin-resistant Staphylococcus aureus IBRS MRSA 011 | cefoxitin | [57] |
Pseudomonas aeruginosa IBRS P001 | penicillin, ampicillin, amoxicillin, tetracycline, neomycin, gentamicin, ceftriaxone | [57] |
P. aeruginosa MMA83 | imipenem, meropenem, gentamycin | [58] |
Escherichia coli IBRS E003 | penicillin, ampicillin, amoxicillin, tetracycline, neomycin, gentamicin, ceftriaxone | [57] |
E. coli IMD989 | amoxicillin/clavulanate, ampicillin/sulbactam, piperacillin/tazobactam, cefuroxime, cefotaxime, ceftazidime, cefepime, imipenem, meropenem, trimethoprim/sulfamethoxazole, amikacin, gentamicin | [59] |
Acinetobacter baumannii 6077/12 | amoxicillin/clavulanate, ampicillin/sulbactam, piperacillin/tazobactam, cefoxitin, cefotaxime, ceftazidime, cefepime, aztreonam, imipenem, meropenem | [60] |
A. baumannii S2/2 | imipenem, meropenem, ciprofloxacin, levofloxacin, amikacin, gentamicin, tobramycin, trimethoprim/sulfamethoxazole, colistin | [61] |
Klebsiella pneumoniae Ni9 | imipenem, meropenem, colistin | [62] |
K. pneumoniae IT977 | ampicillin/clavulanate, piperacillin/tazobactam, cefazolin, ceftriaxone, cefepime, aztreonam, ertapenem, imipenem, meropenem, ciprofloxacin, moxifloxacin, gentamicin, tobramycin, nitrofurantoin | [63] |
Achromobacter xylosoxidans 37F | tetracycline, chloramphenicol, ciprofloxacin, levofloxacin, trimethoprim/sulfamethoxazole | [64] |
Salmonella Infantis 1371/1 | tetracycline, quinolones, colistin | [65] |
Gene | Primer Direction | Sequence (5′-3′) | Amplicon Size (bp) | Reference |
---|---|---|---|---|
lasI | Forward | GCGTGCTCAAGTGTTCAAGG | 125 | [74] |
Reverse | GGGCTTCAGGAGTATCTTCCTGG | |||
lasR | Forward | CTGTGGATGCTCAAGGACTAC | 133 | [75] |
Reverse | AACTGGTCTTGCCGATGG | |||
rhlI | Forward | CCATCCGCAAACCCGCTACATC | 151 | [74] |
Reverse | CTCCCAGACCGACGGATCGCTCGGC | |||
rhlR | Forward | GGGCGTGTTCGCCGTCCTGG | 143 | [74] |
Reverse | GGTATCGCTCCAGCCAGGCCTTG | |||
pqsA | Forward | GACCGGCTGTATTCGATTC | 74 | [75] |
Reverse | GCTGAACCAGGGAAAGAAC | |||
mvfR | Forward | GTCGGGACGGCTACAAGGTCG | 129 | [74] |
Reverse | GATTGCGCGGACCCTTGTTGAG | |||
rpsL | Forward | GCAACTATCAACCAGCTGGTG | 231 | [74] |
Reverse | GCTGTGCTCTTGCAGGTTGTG |
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Ivanov, M.; Novović, K.; Malešević, M.; Dinić, M.; Stojković, D.; Jovčić, B.; Soković, M. Polyphenols as Inhibitors of Antibiotic Resistant Bacteria—Mechanisms Underlying Rutin Interference with Bacterial Virulence. Pharmaceuticals 2022, 15, 385. https://doi.org/10.3390/ph15030385
Ivanov M, Novović K, Malešević M, Dinić M, Stojković D, Jovčić B, Soković M. Polyphenols as Inhibitors of Antibiotic Resistant Bacteria—Mechanisms Underlying Rutin Interference with Bacterial Virulence. Pharmaceuticals. 2022; 15(3):385. https://doi.org/10.3390/ph15030385
Chicago/Turabian StyleIvanov, Marija, Katarina Novović, Milka Malešević, Miroslav Dinić, Dejan Stojković, Branko Jovčić, and Marina Soković. 2022. "Polyphenols as Inhibitors of Antibiotic Resistant Bacteria—Mechanisms Underlying Rutin Interference with Bacterial Virulence" Pharmaceuticals 15, no. 3: 385. https://doi.org/10.3390/ph15030385