Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients

Polyphenols have attracted attention in the fight against antibiotic-resistant bacteria, as they show antibacterial action. Considering that polyphenols inhibit F<sub>1</sub>F<sub>o</sub>-ATP synthase (ATP synthase) and that bacteria need a constant energy production to maint...

Full description

Bibliographic Details
Main Authors: Silvia Ravera, Gabriele Tancreda, Luigi Vezzulli, Anna Maria Schito, Isabella Panfoli
Format: Article
Language:English
Published: MDPI AG 2023-08-01
Series:Molecules
Subjects:
Online Access:https://www.mdpi.com/1420-3049/28/17/6183
_version_ 1797582107333099520
author Silvia Ravera
Gabriele Tancreda
Luigi Vezzulli
Anna Maria Schito
Isabella Panfoli
author_facet Silvia Ravera
Gabriele Tancreda
Luigi Vezzulli
Anna Maria Schito
Isabella Panfoli
author_sort Silvia Ravera
collection DOAJ
description Polyphenols have attracted attention in the fight against antibiotic-resistant bacteria, as they show antibacterial action. Considering that polyphenols inhibit F<sub>1</sub>F<sub>o</sub>-ATP synthase (ATP synthase) and that bacteria need a constant energy production to maintain their homeostasis, we evaluated the effect of two flavones, cirsiliol (tri-hy-droxy-6,7-dimethoxyflavone) and quercetin (3,3,4,5,7-pentahydroxyflavone), on energy production and intracellular ATP content in a methicillin-resistant <i>Staphylococcus aureus</i> (MRSA) strain and a methicillin-resistant <i>Staphylococcus epidermidis</i> (MRSE) strain isolated from patients, comparing the results to those obtained by treating the bacteria with oligomycin, a specific ATP synthase F<sub>o</sub> moiety inhibitor. Real-time quantitative ATP synthesis and total ATP content of permeabilized Gram-positive bacteria were assayed by luminometry. The results showed that cirsiliol and quercetin inhibited ATP synthase and decreased the intracellular ATP levels in both strains, although the effect was higher in MRSE. In addition, while cirsiliol and quercetin acted immediately after the treatment, oligomycin inhibited ATP synthesis only after 30 min of incubation, suggesting that the different responses may depend on the different permeability of the bacterial wall to the three molecules. Thus, cirsiliol and quercetin could be considered potential additions to antibiotics due to their ability to target ATP synthase, against which bacteria cannot develop resistance.
first_indexed 2024-03-10T23:17:10Z
format Article
id doaj.art-3485d73d2b7042049df5893e6291cc62
institution Directory Open Access Journal
issn 1420-3049
language English
last_indexed 2024-03-10T23:17:10Z
publishDate 2023-08-01
publisher MDPI AG
record_format Article
series Molecules
spelling doaj.art-3485d73d2b7042049df5893e6291cc622023-11-19T08:32:27ZengMDPI AGMolecules1420-30492023-08-012817618310.3390/molecules28176183Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from PatientsSilvia Ravera0Gabriele Tancreda1Luigi Vezzulli2Anna Maria Schito3Isabella Panfoli4Department of Experimental Medicine, University of Genoa, 16132 Genoa, ItalyDepartment of Experimental Medicine, University of Genoa, 16132 Genoa, ItalyDepartment of Earth, Environmental and Life Sciences (DISTAV), University of Genoa, Corso Europa 26, 16132 Genoa, ItalyDepartment of Surgical Sciences and Integrated Diagnostics (DISC), University of Genoa, 16132 Genoa, ItalyDepartment of Pharmacy (DIFAR), University of Genoa, 16132 Genoa, ItalyPolyphenols have attracted attention in the fight against antibiotic-resistant bacteria, as they show antibacterial action. Considering that polyphenols inhibit F<sub>1</sub>F<sub>o</sub>-ATP synthase (ATP synthase) and that bacteria need a constant energy production to maintain their homeostasis, we evaluated the effect of two flavones, cirsiliol (tri-hy-droxy-6,7-dimethoxyflavone) and quercetin (3,3,4,5,7-pentahydroxyflavone), on energy production and intracellular ATP content in a methicillin-resistant <i>Staphylococcus aureus</i> (MRSA) strain and a methicillin-resistant <i>Staphylococcus epidermidis</i> (MRSE) strain isolated from patients, comparing the results to those obtained by treating the bacteria with oligomycin, a specific ATP synthase F<sub>o</sub> moiety inhibitor. Real-time quantitative ATP synthesis and total ATP content of permeabilized Gram-positive bacteria were assayed by luminometry. The results showed that cirsiliol and quercetin inhibited ATP synthase and decreased the intracellular ATP levels in both strains, although the effect was higher in MRSE. In addition, while cirsiliol and quercetin acted immediately after the treatment, oligomycin inhibited ATP synthesis only after 30 min of incubation, suggesting that the different responses may depend on the different permeability of the bacterial wall to the three molecules. Thus, cirsiliol and quercetin could be considered potential additions to antibiotics due to their ability to target ATP synthase, against which bacteria cannot develop resistance.https://www.mdpi.com/1420-3049/28/17/6183ATP synthesisF<sub>1</sub>F<sub>o</sub>-ATP synthaseflavonoidsmethicillin-resistant <i>Staphylococcus aureus</i> (MRSA)methicillin-resistant <i>Staphylococcus epidermidis</i> (MRSE)cirsiliol
spellingShingle Silvia Ravera
Gabriele Tancreda
Luigi Vezzulli
Anna Maria Schito
Isabella Panfoli
Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients
Molecules
ATP synthesis
F<sub>1</sub>F<sub>o</sub>-ATP synthase
flavonoids
methicillin-resistant <i>Staphylococcus aureus</i> (MRSA)
methicillin-resistant <i>Staphylococcus epidermidis</i> (MRSE)
cirsiliol
title Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients
title_full Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients
title_fullStr Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients
title_full_unstemmed Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients
title_short Cirsiliol and Quercetin Inhibit ATP Synthesis and Decrease the Energy Balance in Methicillin-Resistant <i>Staphylococcus aureus</i> (MRSA) and Methicillin-Resistant <i>Staphylococcus epidermidis</i> (MRSE) Strains Isolated from Patients
title_sort cirsiliol and quercetin inhibit atp synthesis and decrease the energy balance in methicillin resistant i staphylococcus aureus i mrsa and methicillin resistant i staphylococcus epidermidis i mrse strains isolated from patients
topic ATP synthesis
F<sub>1</sub>F<sub>o</sub>-ATP synthase
flavonoids
methicillin-resistant <i>Staphylococcus aureus</i> (MRSA)
methicillin-resistant <i>Staphylococcus epidermidis</i> (MRSE)
cirsiliol
url https://www.mdpi.com/1420-3049/28/17/6183
work_keys_str_mv AT silviaravera cirsiliolandquercetininhibitatpsynthesisanddecreasetheenergybalanceinmethicillinresistantistaphylococcusaureusimrsaandmethicillinresistantistaphylococcusepidermidisimrsestrainsisolatedfrompatients
AT gabrieletancreda cirsiliolandquercetininhibitatpsynthesisanddecreasetheenergybalanceinmethicillinresistantistaphylococcusaureusimrsaandmethicillinresistantistaphylococcusepidermidisimrsestrainsisolatedfrompatients
AT luigivezzulli cirsiliolandquercetininhibitatpsynthesisanddecreasetheenergybalanceinmethicillinresistantistaphylococcusaureusimrsaandmethicillinresistantistaphylococcusepidermidisimrsestrainsisolatedfrompatients
AT annamariaschito cirsiliolandquercetininhibitatpsynthesisanddecreasetheenergybalanceinmethicillinresistantistaphylococcusaureusimrsaandmethicillinresistantistaphylococcusepidermidisimrsestrainsisolatedfrompatients
AT isabellapanfoli cirsiliolandquercetininhibitatpsynthesisanddecreasetheenergybalanceinmethicillinresistantistaphylococcusaureusimrsaandmethicillinresistantistaphylococcusepidermidisimrsestrainsisolatedfrompatients