Inhibition of ATPase activity of Escherichia coli ATP synthase by polyphenols

Dadi, Prasanna K.; Ahmad, Mubeen; Ahmad, Zulfiqar

doi:10.1016/j.ijbiomac.2009.04.004

Cited by 111 publications

(144 citation statements)

References 64 publications

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“…Consequently, MccPDI activity correlates with the presence of a functional ATP synthase complex. To determine if a functional ATP synthase is required for susceptibility, we conducted competition experiments in the presence of a previously described ATP synthase inhibitor, the polyphenol resveratrol (8). Inhibition of ATP synthase activity resulted in reduced susceptibility to MccPDI (see Fig.…”

Section: Resultsmentioning

confidence: 99%

See 1 more Smart Citation

Genome-Wide Screening Identifies Six Genes That Are Associated with Susceptibility to Escherichia coli Microcin PDI

Zhao

Eberhart

Orfe

et al. 2015

Appl Environ Microbiol

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The microcin PDI inhibits a diverse group of pathogenic Escherichia coli strains. Coculture of a single-gene knockout library (BW25113; n ‫؍‬ 3,985 mutants) against a microcin PDI-producing strain (E. coli 25) identified six mutants that were not susceptible (⌬atpA, ⌬atpF, ⌬dsbA, ⌬dsbB, ⌬ompF, and ⌬ompR). Complementation of these genes restored susceptibility in all cases, and the loss of susceptibility was confirmed through independent gene knockouts in E. coli O157:H7 Sakai. Heterologous expression of E. coli ompF conferred susceptibility to Salmonella enterica and Yersinia enterocolitica strains that are normally unaffected by microcin PDI. The expression of chimeric OmpF and site-directed mutagenesis revealed that the K 47 G 48 N 49 region within the first extracellular loop of E. coli OmpF is a putative binding site for microcin PDI. OmpR is a transcriptional regulator for ompF, and consequently loss of susceptibility by the ⌬ompR strain most likely is related to this function. Deletion of AtpA and AtpF, as well as AtpE and AtpH (missed in the original library screen), resulted in the loss of susceptibility to microcin PDI and the loss of ATP synthase function. Coculture of a susceptible strain in the presence of an ATP synthase inhibitor resulted in a loss of susceptibility, confirming that a functional ATP synthase complex is required for microcin PDI activity. In trans expression of ompF in the ⌬dsbA and ⌬dsbB strains did not restore a susceptible phenotype, indicating that these proteins are probably involved with the formation of disulfide bonds for OmpF or microcin PDI. E scherichia coli strain 25 (E. coli 25; cattle origin) has an in vitro and in vivo competitive advantage against other E. coli strains that is linked to the production of the microcin PDI (MccPDI) (1-3). The inhibitory phenotype was first observed in vitro (4) and later called "proximity-dependent inhibition" (PDI), because inhibition occurred only when competing cells were in close proximity to sensitive cells (1). MccPDI appears to be most closely related to class IIa microcins, and the cluster of genes that encode MccPDI and associated immunity, activation, and export are located on a conjugative plasmid (2).E. coli produces various antimicrobial bacteriocins that are classified as colicins or microcins. Microcins are distinguished by their lower molecular mass (Ͻ10 kDa) and require active transport across the membrane of producing cells. Microcins typically have a narrow spectrum of activity that is mediated through specific receptors expressed on the surface of susceptible bacteria. To date, 16 microcins have been described, including MccPDI. The receptors for seven of these microcins have been identified and include the outer membrane proteins Cir, FepA, Fiu, FhuA, and OmpF, all of which normally function in iron and other nutrient uptake (5-7).While the gene encoding MccPDI has been identified and gene knockout and complementation studies have confirmed its inhibitory activity (2), little is known about how this microcin functi...

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Section: Resultsmentioning

confidence: 99%

“…Monocultures of each competing strain also were prepared as controls after inoculation into fresh M9 medium at the same dilution. The ATP synthase inhibitor resveratrol (Sigma-Alrich) was added at a final concentration of 25 g ml Ϫ1 to determine if a functional ATP synthase complex is required for susceptibility to MccPDI (8).…”

Section: Methodsmentioning

confidence: 99%

Genome-Wide Screening Identifies Six Genes That Are Associated with Susceptibility to Escherichia coli Microcin PDI

Zhao

Eberhart

Orfe

et al. 2015

Appl Environ Microbiol

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“…These microdomains sequester the polyphenol, as described recently for autocrine motility factor (AMF)/phosphoglucose isomerase (PGI)-paclitaxel (46), and therefore function as a platform that finely tunes up the tumor cell response to this agent, either directly by inducing cell-cycle arrest or cell death (47) or indirectly by sensitizing the cells to chemotherapeutic agents (11,15). This sensitization could involve the inhibition of the H þ -ATP synthase by resveratrol (48). Similarly to the proton pump inhibitor omeprazole (49), resveratrol could affect the lysosomal function and reduce cell environment acidity, thereby facilitating the drug activity (50).…”

Section: Discussionmentioning

confidence: 98%

Endocytosis of Resveratrol via Lipid Rafts and Activation of Downstream Signaling Pathways in Cancer Cells

Colin

Limagne²,

Jeanningros³

et al. 2011

Cancer Prevention Research

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trans-Resveratrol has been proposed to prevent tumor growth and to sensitize cancer cells to anticancer agents. Polyphenol entry into the cells has remained poorly understood. Here, we show that [ 3 H]-resveratrol enters colon cancer cells (SW480, SW620, HT29) and leukemia U937 cells through a monensin (5-20 mmol/L) -sensitive process that suggests clathrin-independent endocytosis. Uptake of the molecule can be prevented by methyl-b-cyclodextrin (2-12 mg/mL), nystatin (12 ng/mL), and filipin (1 mg/mL), which all disrupt plasma membrane lipid rafts. Accordingly, radiolabeled resveratrol accumulates in sphingomyelin-and cholesterol-enriched cell fractions. Interestingly, extracellular signalregulated kinases (ERK), c-Jun NH 2 -terminal kinases (JNK), and Akt also accumulate in lipid rafts on resveratrol exposure (IC 50 at 48 h % 30 mmol/L in SW480 and U937 cells). In these rafts also, resveratrol promotes the recruitment, by the integrin a V b 3 (revealed by coimmunoprecipitation with an anti-integrin a V b 3 antibody), of signaling molecules that include the FAK (focal adhesion kinase), Fyn, Grb2, Ras, and SOS proteins. Resveratrol-induced activation of downstream signaling pathways and caspase-dependent apoptosis is prevented by endocytosis inhibitors, lipid raft-disrupting molecules, and the integrin antagonist peptide arginine-glycine-aspartate (500 nmol/L). Altogether, these data show the role played by lipid rafts in resveratrol endocytosis and activation of downstream pathways leading to cell death.

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“…1A), are known inhibitors of F 1 -ATPase, except that Bacillus PS3 F 1 is insensitive (21,25). We determined their effects on the bulk phase steady-state ATPase of E. coli wildtype F 1 as well as the modified complex that was engineered for direct observation of rotation behavior.…”

Section: Effects Of Piceatannol On Bulk Phasementioning

confidence: 99%

Binding of Phytopolyphenol Piceatannol Disrupts β/γ Subunit Interactions and Rate-limiting Step of Steady-state Rotational Catalysis in Escherichia coli F1-ATPase

Sekiya

Nakamoto

Nakanishi‐Matsui

et al. 2012

Journal of Biological Chemistry

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Background:The ␤/␥ subunit interactions are critical for rotational catalysis in ATP synthase. Results: Piceatannol increases the activation energy for the rate-limiting transition state. Conclusion: Piceatannol binding and a ␤/␥ subunit interface mutation, although the sites are physically separated, affect the same rate-limiting transition-state step. Significance: Multiple rotor-stator interactions contribute to formation of the transition state.

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Inhibition of ATPase activity of Escherichia coli ATP synthase by polyphenols

Cited by 111 publications

References 64 publications

Genome-Wide Screening Identifies Six Genes That Are Associated with Susceptibility to Escherichia coli Microcin PDI

Genome-Wide Screening Identifies Six Genes That Are Associated with Susceptibility to Escherichia coli Microcin PDI

Endocytosis of Resveratrol via Lipid Rafts and Activation of Downstream Signaling Pathways in Cancer Cells

Binding of Phytopolyphenol Piceatannol Disrupts β/γ Subunit Interactions and Rate-limiting Step of Steady-state Rotational Catalysis in Escherichia coli F1-ATPase

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