Interactions of Galloylated Polyphenols with a Simple Gram-Negative Bacterial Membrane Lipid Model

Overview

Journal Membranes (Basel)

Date 2024 Feb 23

PMID 38392674

Authors

Ryan T Coones

Maarit Karonen

Rebecca J Green

Richard Frazier

Affiliations

Soon will be listed here.

Abstract

Differential scanning calorimetry (DSC) was used to explore the interactions of isolated polyphenolic compounds, including (-)-epigallocatechin gallate ((-)-EGCg), tellimagrandins I and II (Tel-I and Tel-II), and 1,2,3,4,6-penta--galloyl-d-glucose (PGG), with a model Gram-negative bacterial membrane with a view to investigating their antimicrobial properties. The model membranes comprised 1,2-dipalmitoyl-sn-glycero-3-phosphoethanolamine (DPPE) and 1,2-dipalmitoyl-sn-glycero-3-phospho-(1'-rac-glycerol) (DPPG), fabricated to mimic the domain formation observed in natural membranes, as well as ideally mixed lipid vesicles for the interaction with (-)-EGCg. Polyphenols induced changes in lipid mixing/de-mixing depending on the method of vesicle preparation, as was clearly evidenced by alterations in the lipid transition temperatures. There was a distinct affinity of the polyphenols for the DPPG lipid component, which was attributed to the electrostatic interactions between the polyphenolic galloyl moieties and the lipid headgroups. These interactions were found to operate through either the stabilization of the lipid headgroups by the polyphenols or the insertion of the polyphenols into the membrane itself. Structural attributes of the polyphenols, including the number of galloyl groups, the hydrophobicity quantified by partition coefficients (logP), and structural flexibility, exhibited a correlation with the temperature transitions observed in the DSC measurements. This study furthers our understanding of the intricate interplay between the structural features of polyphenolic compounds and their interactions with model bacterial membrane vesicles towards the exploitation of polyphenols as antimicrobials.

References

Tanaka T, Zhang H, Jiang Z, Kouno I . Relationship between hydrophobicity and structure of hydrolyzable tannins, and association of tannins with crude drug constituents in aqueous solution. Chem Pharm Bull (Tokyo). 1998; 45(12):1891-7. DOI: 10.1248/cpb.45.1891. View

Schwieger C, Blume A . Interaction of poly(L-lysines) with negatively charged membranes: an FT-IR and DSC study. Eur Biophys J. 2006; 36(4-5):437-50. DOI: 10.1007/s00249-006-0080-8. View

Virtanen V, Green R, Karonen M . Interactions between Hydrolysable Tannins and Lipid Vesicles from with Isothermal Titration Calorimetry. Molecules. 2022; 27(10). PMC: 9146631. DOI: 10.3390/molecules27103204. View

Virtanen V, Raikkonen S, Puljula E, Karonen M . Ellagitannin-Lipid Interaction by HR-MAS NMR Spectroscopy. Molecules. 2021; 26(2). PMC: 7828275. DOI: 10.3390/molecules26020373. View

Li A, Li S, Zhang Y, Xu X, Chen Y, Li H . Resources and biological activities of natural polyphenols. Nutrients. 2014; 6(12):6020-47. PMC: 4277013. DOI: 10.3390/nu6126020. View

Sirk T, Brown E, Sum A, Friedman M . Molecular dynamics study on the biophysical interactions of seven green tea catechins with lipid bilayers of cell membranes. J Agric Food Chem. 2008; 56(17):7750-8. DOI: 10.1021/jf8013298. View

Nakayama T, Hashimoto T, Kajiya K, Kumazawa S . Affinity of polyphenols for lipid bilayers. Biofactors. 2001; 13(1-4):147-51. DOI: 10.1002/biof.5520130124. View

Colina J, Suwalsky M, Manrique-Moreno M, Petit K, Aguilar L, Jemiola-Rzeminska M . Protective effect of epigallocatechin gallate on human erythrocytes. Colloids Surf B Biointerfaces. 2018; 173:742-750. DOI: 10.1016/j.colsurfb.2018.10.038. View

Karonen M . Insights into Polyphenol-Lipid Interactions: Chemical Methods, Molecular Aspects and Their Effects on Membrane Structures. Plants (Basel). 2022; 11(14). PMC: 9317924. DOI: 10.3390/plants11141809. View

10.

Clifton L, Hall S, Mahmoudi N, Knowles T, Heinrich F, Lakey J . Structural Investigations of Protein-Lipid Complexes Using Neutron Scattering. Methods Mol Biol. 2019; 2003:201-251. DOI: 10.1007/978-1-4939-9512-7_11. View

11.

Lohner K, Prenner E . Differential scanning calorimetry and X-ray diffraction studies of the specificity of the interaction of antimicrobial peptides with membrane-mimetic systems. Biochim Biophys Acta. 1999; 1462(1-2):141-56. DOI: 10.1016/s0005-2736(99)00204-7. View

12.

Nassarawa S, Nayik G, Gupta S, Areche F, Jagdale Y, Javed Ansari M . Chemical aspects of polyphenol-protein interactions and their antibacterial activity. Crit Rev Food Sci Nutr. 2022; 63(28):9482-9505. DOI: 10.1080/10408398.2022.2067830. View

13.

Simons K, Vaz W . Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct. 2004; 33:269-95. DOI: 10.1146/annurev.biophys.32.110601.141803. View

14.

Virtanen V, Karonen M . Partition Coefficients () of Hydrolysable Tannins. Molecules. 2020; 25(16). PMC: 7465006. DOI: 10.3390/molecules25163691. View

15.

Matsuzaki T, Ito H, Chevyreva V, Makky A, Kaufmann S, Okano K . Adsorption of galloyl catechin aggregates significantly modulates membrane mechanics in the absence of biochemical cues. Phys Chem Chem Phys. 2017; 19(30):19937-19947. DOI: 10.1039/c7cp02771k. View

16.

Puljula E, Walton G, Woodward M, Karonen M . Antimicrobial Activities of Ellagitannins against , , and . Molecules. 2020; 25(16). PMC: 7465317. DOI: 10.3390/molecules25163714. View

17.

Quideau S, Deffieux D, Douat-Casassus C, Pouysegu L . Plant polyphenols: chemical properties, biological activities, and synthesis. Angew Chem Int Ed Engl. 2011; 50(3):586-621. DOI: 10.1002/anie.201000044. View

18.

Nie R, Dang M, Ge Z, Huo Y, Yu B, Tang S . Influence of the gallate moiety on the interactions between green tea polyphenols and lipid membranes elucidated by molecular dynamics simulations. Biophys Chem. 2021; 274:106592. DOI: 10.1016/j.bpc.2021.106592. View

19.

Kajiya K, Kumazawa S, Naito A, Nakayama T . Solid-state NMR analysis of the orientation and dynamics of epigallocatechin gallate, a green tea polyphenol, incorporated into lipid bilayers. Magn Reson Chem. 2007; 46(2):174-7. DOI: 10.1002/mrc.2157. View

20.

Sohlenkamp C, Geiger O . Bacterial membrane lipids: diversity in structures and pathways. FEMS Microbiol Rev. 2015; 40(1):133-59. DOI: 10.1093/femsre/fuv008. View