Membrane interactions of phytochemicals as their molecular mechanism applicable to the discovery of drug leads from plants

Molecules

Volumn 20, Issue 10, 2015, Pages 18923-18966

  Tsuchiya, Hironori ^a  

^a ASAHI UNIVERSITY   (Japan)

Author keywords

Drug lead; Membrane fluidity; Membrane interaction; Molecular mechanism; Phytochemical

Indexed keywords

CAPSAICIN; FLAVONOID; PLANT EXTRACT; STILBENE DERIVATIVE; TERPENE;

ANIMAL; CELL MEMBRANE; DRUG DEVELOPMENT; DRUG EFFECTS; HUMAN; METABOLISM;

ANIMALS; CAPSAICIN; CELL MEMBRANE; DRUG DISCOVERY; FLAVONOIDS; HUMANS; PLANT EXTRACTS; STILBENES; TERPENES;

EID: 84947767274     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules201018923     Document Type: Article

References (163)

1. Lee, K.H. Discovery and development of natural product-derived chemotherapeutic agents based on a medicinal chemistry approach. J. Nat. Prod. 2010, 73, 500-516.
2. Tapsell, L.C.; Hemphill, I.; Cobiac, L.; Patch, C.S.; Sullivan, D.R.; Fenech, M.; Roodenrys, S.; Keogh, J.B.; Clifton, P.M.; Williams, P.G.; et al. Health benefits of herbs and spices: The past, the present, the future. Med. J. Aust. 2006, 185, S4-S24.
3. Kopeć, W.; Telenius, J.; Khandelia, H. Molecular dynamics simulations of the interactions of medicinal plant extracts and drugs with lipid bilayer membranes. FEBS J. 2013, 280, 2785-2805.
4. Lúcio, M.; Lima, J.L.; Reis, S. Drug-membrane interactions: Significance for medicinal chemistry. Curr. Med. Chem. 2010, 17, 1795-1809.
5. Tsuchiya, H.; Mizogami, M. Interaction of local anesthetics with biomembranes consisting of phospholipids and cholesterol: Mechanistic and clinical implications for anesthetic and cardiotoxic effects. Anesthesiol. Res. Pract. 2013, doi:10.1155/2013/297141.
6. Tsuchiya, H. Structure-specific membrane-fluidizing effect of propofol. Clin. Exp. Pharmacol. Physiol. 2001, 28, 292-299.
7. Bahri, M.A.; Heyne, B.J.; Hans, P.; Seret, A.E.; Mouithys-Mickalad, A.A.; Hoebeke, M.D. Quantification of lipid bilayer effective microviscosity and fluidity effect induced by propofol. Biophys. Chem. 2005, 114, 53-61.
8. Hauet, N.; Artzner, F.; Boucher, F.; Grabielle-Madelmont, C.; Cloutier, I.; Keller, G.; Lesieur, P.; Durand, D.; Paternostre, M. Interaction between artificial membranes and enflurane, a general volatile anesthetic: DPPC-enflurane interaction. Biophys. J. 2003, 84, 3123-3137.
9. Booker, R.D.; Sun, A.K. Biophysical changes induced by xenon on phospholipid bilayers. Biochim. Biophys. Acta 2013, 1828, 1347-1356.
10. Harris, R.A.; Schroeder, F. Effects of barbiturates and ethanol on the physical properties of brain membranes. J. Pharmacol. Exp. Ther. 1982, 223, 424-431.
11. Mennini, T.; Ceci, A.; Caccia, S.; Garattini, S.; Masturzo, P.; Salmona, M. Diazepam increases membrane fluidity of rat hippocampus synaptosomes. FEBS Lett. 1984, 173, 255-258.
12. Jerabek, H.; Pabst, G.; Rappolt, M.; Stockner, T. Membrane-mediated effect on ion channels induced by the anesthetic drug ketamine. J. Am. Chem. Soc. 2010, 132, 7990-7997.
13. Søgaard, R.; Werge, T.M.; Bertelsen, C.; Lundbye, C.; Madsen, K.L.; Nielsen, C.H.; Lundbaek, J.A. GABAA receptor function is regulated by lipid bilayer elasticity. Biochemistry 2006, 45, 13118-13129.
14. Mizogami, M.; Tsuchiya, H.; Harada, J. Membrane effects of ropivacaine compared with those of bupivacaine and mepivacaine. Fundam. Clin. Pharmacol. 2002, 16, 325-330.
15. Tsuchiya, H.; Mizogami, M. Membrane interactivity of charged local anesthetic derivative and stereoselectivity in membrane interaction of local anesthetic enantiomers. Local Reg. Anesth. 2008, 1, 1-9.
16. Lorite, G.S.; Nobre, T.M.; Zaniquelli, M.E.; de Paula, E.; Cotta, M.A. Dibucaine effects on structural and elastic properties of lipid bilayers. Biophys. Chem. 2009, 139, 75-83.
17. Yi, Z.; Nagao, M.; Bossev, D.P. Effect of charged lidocaine on static and dynamic properties of model bio-membranes. Biophys. Chem. 2012, 160, 20-27.
18. Lundbaek, J.A. Lipid bilayer-mediated regulation of ion channel function by amphiphilic drugs. J. Gen. Physiol. 2008, 131, 421-429.
19. Leifert, W.R.; McMurchie, E.J.; Saint, D.A. Inhibition of cardiac sodium currents in adult rat myocytes by n-3 polyunsaturated fatty acids. J. Physiol. 1999, 520 Pt 3, 671-679.
20. Hahin, R.; Larsen, J.; Gasser, K. Predictions of the EC50 for action potential block for aliphatic solutes. J. Membr. Biol. 2008, 221, 73-85.
21. Lundbaek, J.A.; Birn, P.; Tape, S.E.; Toombes, G.E.; Søgaard, R.; Koeppe, R.E. II; Gruner, S.M.; Hansen, A.J.; Andersen, O.S. Capsaicin regulates voltage-dependent sodium channels by altering lipid bilayer elasticity. Mol. Pharmacol. 2005, 68, 680-689.
22. Frangopol, P.T.; Mihəilescu, D. Interactions of some local anesthetics and alcohols with membranes. Colloids Surf. B Biointerfaces 2001, 22, 3-22.
23. Tsuchiya, H.; Mizogami, M. R(+)-, Rac-, and S(-)-bupivacaine stereostructure-specifically interact with membrane lipids at cardiotoxically relevant concentrations. Anesth. Analg. 2012, 114, 310-312.
24. Cantor, R.S. Receptor desensitization by neurotransmitters in membranes: Are neurotransmitters the endogenous anesthetics? Biochemistry 2003, 42, 11891-11897.
25. Lombardi, D.; Cuenoud, B.; Krämer, S.D. Lipid membrane interactions of indacaterol and salmeterol: Do they influence their pharmacological properties? Eur. J. Pharm. Sci. 2009, 38, 533-547.
26. Butler, S.; Wang, R.; Wunder, S.L.; Cheng, H.Y.; Randall, C.S. Perturbing effects of carvedilol on a model membrane system: Role of lipophilicity and chemical structure. Biophys. Chem. 2006, 119, 307-315.
27. Mizogami, M.; Takakura, K.; Tsuchiya, H. The interactivities with lipid membranes differentially characterize selective and nonselective β1-blockers. Eur. J. Anaesthesiol. 2010, 27, 829-834.
28. Tsuchiya, H.; Mizogami, M. Characteristic interactivity of landiolol, an ultra-short-acting highly selective β1-blocker, with biomimetic membranes: Comparisons with β1-selective esmolol and non-selective propranolol and alprenolol. Front. Pharmacol. 2013, doi:10.3389/fphar.2013.00150.
29. Cheng, H.Y.; Randall, C.S.; Holl, W.W.; Constantinides, P.P.; Yue, T.L.; Feuerstein, G.Z. Carvedilol-liposome interaction: Evidence for strong association with the hydrophobic region of the lipid bilayers. Biochim. Biophys. Acta 1996, 1284, 20-28.
30. Manevich, E.M.; Köiv, A.; Järv, J.; Molotkovsky, J.G.; Bergelson, L.D. Binding to specific ligands to muscarinic receptors alters the fluidity of membrane fragments from rat brain. A fluorescence polarization study with lipid-specific probes. FEBS. Lett. 1988, 236, 43-46.
31. Tang, C.; Castoldi, A.F.; Costa, L.G. Effects of the muscarinic agonist oxotremorine on membrane fluidity in rat lymphocytes. Biochem. Mol. Biol. Int. 1993, 29, 1047-1054.
32. Lichtenberger, L.M.; Zhou, Y.; Jayaraman, V.; Doyen, J.R.; O'Neil, R.G.; Dial, E.J.; Volk, D.E.; Gorenstein, D.G.; Boggara, M.B.; Krishnamoorti, R. Insight into NSAID-induced membrane alterations, pathogenesis and therapeutics: Characterization of interaction of NSAIDs with phosphatidylcholine. Biochim. Biophys. Acta 2012, 1821, 994-1002.
33. Rand Doyen, J.; Yucer, N.; Lichtenberger, L.M.; Kulmacz, R.J. Phospholipid actions on PGHS-1 and -2 cyclooxygenase kinetics. Prostaglandins Other Lipid Mediat. 2008, 85, 134-143.
34. Alsop, R.J.; Barrett, M.A.; Zheng, S.; Dies, H.; Rheinstädter, M.C. Acetylsalicylic acid (ASA) increases the solubility of cholesterol when incorporated in lipid membranes. Soft Matter. 2014, 10, 4275-4286.
35. Alsop, R.J.; Toppozini, L.; Marquardt, D.; Kučerka, N.; Harroun, T.A.; Rheinstädter, M.C. Aspirin inhibits formation of cholesterol rafts in fluid lipid membranes. Biochim. Biophys. Acta 2015, 1848, 805-812.
36. Manrique-Moreno, M.; Garidel, P.; Suwalsky, M.; Howe, J.; Brandenburg, K. The membrane-activity of Ibuprofen, Diclofenac, and Naproxen: A physic-chemical study with lecithin phospholipids. Biochim. Biophys. Acta 2009, 1788, 1296-1303.
37. Abramson, S.B.; Cherksey, B.; Gude, D.; Leszczynska-Piziak, J.; Phillips, M.R.; Blau, L.; Weissmann, G. Nonsteroidal anti-inflammatory drugs exert differential effects on neutrophil function and plasma membrane viscosity. Studies in human neutrophils and liposomes. Inflammation 1990, 14, 11-30.
38. Winocour, P.D.; Watala, C.; Perry, D.W.; Kinlough-Rathbone, R.L. Decreased platelet membrane fluidity due to glycation or acetylation of membrane proteins. Thromb. Haemost. 1992, 68, 577-582.
39. Song, Y.; Guallar, V.; Baker, N.A. Molecular dynamics simulations of salicylate effects on the micro- and mesoscopic properties of a dipalmitoylphosphatidylcholine bilayer. Biochemistry 2005, 44, 13425-13438.
40. Khandelia, H.; Witzke, S.; Mouritsen, O.G. Interaction of salicylate and a terpenoid plant extract with model membranes: Reconciling experiments and simulations. Biophys. J. 2010, 99, 3887-3894.
41. Lúcio, M.; Ferreira, H.; Lima, J.L.; Reis, S. Interactions between oxicams and membrane bilayers: An explanation for their different COX selectivity. Med. Chem. 2006, 2, 447-456.
42. Tavolari, S.; Munarini, A.; Storci, G.; Laufer, S.; Chieco, P.; Guarnieri, T. The decrease of cell membrane fluidity by the non-steroidal anti-inflammatory drug licofelone inhibits epidermal growth factor receptor signalling and triggers apoptosis in HCA-7 colon cancer cells. Cancer Lett. 2012, 321, 187-194.
43. Sade, A.; Tunçay, S.; Cimen, I.; Severcan, F.; Banerjee, S. Celecoxib reduces fluidity and decreases metastatic potential of colon cancer cell lines irrespective of COX-2 expression. Biosci. Rep. 2012, 32, 35-44.
44. Nunes, C.; Lopes, D.; Pinheiro, M.; Pereira-Leite, C.; Reis, S. In vitro assessment of NSAIDs-membrane interactions: Significance for pharmacological actions. Pharm. Res. 2013, 30, 2097-2107.
45. Nie, X.; Wen, Z.Y.; Yan, Z.Y.; Huang, L.; Sun, D.; Cheng, B. Effects of morphine on rheological properties of rat red blood cells. Clin. Hemorheol. Microcirc. 2000, 22, 189-195.
46. García, D.A.; Bujons, J.; Vale, C.; Suñol, C. Allosteric positive interaction of thymol with the GABAA receptor in primary cultures of mouse cortical neurons. Neuropharmacology 2006, 50, 25-35.
47. Tsuchiya, H.; Mizogami, M. Comparative interactions of anesthetic alkylphenols with lipid membranes. Open J. Anesthesiol. 2014, 4, 308-317.
48. Daoud, S.S. Cell membranes as targets for anti-cancer drug action. Anticancer Drugs 1992, 3, 443-453.
49. Muller, C.P.; Krueger, G.R. Modulation of membrane proteins by vertical phase separation and membrane lipid fluidity. Basis for a new approach to tumor immunotherapy. Anticancer Res. 1986, 6, 1181-1193.
50. Czapla, K.; Korchowiec, B.; Rogalska, E. Differentiating oxicam nonsteroidal anti-inflammatory drugs in phosphoglyceride monolayers. Langmuir 2010, 26, 3485-3492.
51. Baritaki, S.; Apostolakis, S.; Kanellou, P.; Dimanche-Boitrel, M.T.; Spandidos, D.A.; Bonavida, B. Reversal of tumor resistance to apoptotic stimuli by alteration of membrane fluidity: Therapeutic implications. Adv. Cancer Res. 2007, 98, 149-190.
52. Dimanche-Boitrel, M.T.; Meurette, O.; Rebillard, A.; Lacour, S. Role of early plasma membrane events in chemotherapy-induced cell death. Drug Resist. Updat. 2005, 8, 5-14.
53. Rebillard, A.; Lagadic-Gossmann, D.; Dimanche-Boitrel, M.T. Cisplatin cytotoxicity: DNA and plasma membrane targets. Curr. Med. Chem. 2008, 15, 2656-2663.
54. Marutaka, M.; Iwagaki, H.; Suguri, T.; Tanaka, N.; Orita, K. Alterations of membrane fluidity in K562 cells exposed to the anticancer drug adriamycin. Res. Commun. Mol. Pathol. Pharmacol. 1994, 85, 163-170.
55. Marczak, A.; Kowalczyk, A.; Wrzesień-Kus̈, A.; Robak, T.; Jóźwiak, Z. Interaction of doxorubicin and idarubicin with red blood cells from acute myeloid leukemia patients. Cell Biol. Int. 2006, 30, 127-132.
56. Mandlekar, S.; Kong, A.N. Mechanisms of tamoxifen-induced apoptosis. Apoptosis 2001, 6, 469-477.
57. Cronier, F.; Patenaude, A.; C-Gaudreault, R.; Auger, M. Membrane composition modulates the interaction between a new class of antineoplastic agents deriving from aromatic 2-chloroethylureas and lipid bilayers: A solid-state NMR study. Chem. Phys. Lipids 2007, 146, 125-135.
58. Grunicke, H.; Grünewald, K.; Helliger, W.; Scheidl, F.; Wolff-Schreiner, E.; Puschendorf, B. Inhibition of tumor growth by an alkylation of the plasma membrane. Adv. Enzyme Regul. 1983, 21, 21-30.
59. Bernsdorff, C.; Reszka, R.; Winter, R. Interaction of the anticancer agent Taxol (paclitaxel) with phospholipid bilayers. J. Biomed. Mater. Res. 1999, 46, 141-149.
60. Houari, A.; di Martino, P. Effect of chlorhexidine and benzalkonium chloride on bacterial biofilm formation. Lett. Appl. Microbiol. 2007, 45, 652-656.
61. Takasaki, A.; Hashida, T.; Kato, K.; Moriyama, T.; Nishihara, T. Action of a quaternary ammonium disinfectant on cell membrane of Staphylococcus aureus. Jpn. J. Toxicol. Environ. Health 1994, 40, 520-526.
62. Bensikaddour, H.; Snoussi, K.; Lins, L.; van Bambeke, F.; Tulkens, P.M.; Brasseur, R.; Goormaghtigh, E.; Mingeot-Leclercq, M.P. Interactions of ciprofloxacin with DPPC and DPPG: Fluorescence anisotropy, ATR-FTIR and 31P NMR spectroscopies and conformational analysis. Biochim. Biophys. Acta 2008, 1778, 2535-2543.
63. Van Bambeke, F.; Mingeot-Leclercq, M.P.; Schanck, A.; Brasseur, R.; Tulkens, P.M. Alterations in membrane permeability induced by aminoglycoside antibiotics: Studies on liposomes and cultured cells. Eur. J. Pharmacol. 1993, 247, 155-168.
64. Berquand, A.; Fa, N.; Dufrêne, Y.F.; Mingeot-Leclercq, M.P. Interaction of the macrolide antibiotic azithromycin with lipid bilayers: Effect on membrane organization, fluidity, and permeability. Pharm. Res. 2005, 22, 465-475.
65. Tyteca, D.; Schanck, A.; Dufrêne, Y.F.; Deleu, M.; Courtoy, P.J.; Tulkens, P.M.; Mingeot-Leclercq, M.P. The macrolide antibiotic azithromycin interacts with lipids and affects membrane organization and fluidity: Studies on Langmuir-Blodgett monolayers, liposomes and J774 macrophages. J. Membr. Biol. 2003, 192, 203-215.
66. Yasui, K.; Masuda, M.; Matsuoka, T.; Yamazaki, M.; Komiyama, A.; Akabane, T.; Murata, K. Miconazole and amphotericin B alter polymorphonuclear leukocyte functions and membrane fluidity in similar fashions. Antimicrob. Agents Chemother. 1988, 32, 1864-1868.
67. Virág, E.; Belagyi, J.; Gazdag, Z.; Vágvölgyi, C.; Pesti, M. Direct in vivo interaction of the antibiotic primycin with the plasma membrane of Candida albicans: An EPR study. Biochim. Biophys. Acta 2012, 1818, 42-48.
68. Tai, W.Y.; Yang, Y.C.; Lin, H.J.; Huang, C.P.; Cheng, Y.L.; Chen, M.F.; Yen, H.L.; Liau, I. Interplay between structure and fluidity of model lipid membranes under oxidative attack. J. Phys. Chem. B 2010, 114, 15642-15649.
69. Tsuchiya, H. Lipid peroxidation-inhibitory effects of perioperatively used drugs associated with their membrane interactions. Oxid. Antioxid. Med. Sci. 2014, 3, 91-98.
70. Lúcio, M.; Ferreira, H.; Lima. J.L.; Reis, S. Use of liposomes to evaluate the role of membrane interactions on antioxidant activity. Anal. Chim. Acta 2007, 597, 163-170.
71. Gutiérrez, M.E.; García, A.F.; Africa de Madariaga, M.; Sagrista, M.L.; Casadó, F.J.; Mora, M. Interaction of tocopherols and phenolic compounds with membrane lipid components: Evaluation of their antioxidant activity in a liposomal model system. Life Sci. 2003, 72, 2337-2360.
72. Arora, A.; Byrem, T.M.; Nair, M.G.; Strasburg, G.M. Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Arch. Biochem. Biophys. 2000, 373, 102-109.
73. Vlasic, N.; Medow, M.S.; Schwarz, S.M.; Pritchard, K.A., Jr.; Stemerman, M.B. Lipid fluidity modulates platelet aggregation and agglutination in vitro. Life Sci. 1993, 53, 1053-1060.
74. Rao, G.H.; White, J.G. Disaggregation and reaggregation of "irreversibly" aggregated platelets: A method for more complete evaluation of anti-platelet drugs. Agents Actions 1985, 16, 425-434.
75. Sheu, J.R.; Hung, W.C.; Lee, L.W.; Chang, P.T.; Kan, Y.C.; Yen, M.H. Mechanism involved in the antiplatelet activity of naloxone in human platelets. Biochem. Biophys. Res. Commun. 1997, 231, 12-16.
76. Matera, C.; Falzarano, C.; Vacca, C.; Falciani, M.; Rossi, F. Effects of some antineoplastic drugs (vincristine, doxorubicin and epirubicin) on human platelet aggregation. J. Med. 1994, 25, 2-16.
77. Chang, Y.; Chen, T.L.; Wu, G.J.; Hsiao, G.; Shen, M.Y.; Lin, K.H.; Chou, D.S.; Lin, C.H.; Sheu, J.R. Mechanisms involved in the antiplatelet activity of ketamine in human platelets. J. Biomed. Sci. 2004, 11, 764-772.
78. Sheu, J.R.; Hsiao, G.; Luk, H.N.; Chen, Y.W.; Chen, T.L.; Lee, L.W.; Lin, C.H.; Chou, D.S. Mechanisms involved in the antiplatelet activity of midazolam in human platelets. Anesthesiology 2002, 96, 651-658.
79. Tsuchiya, H. Effects of red wine flavonoid components on biomembranes and cell proliferation. Int. J. Wine Res. 2011, 3, 9-17.
80. Wu, T.; He, M.; Zang, X.; Zhou, Y.; Qiu, T.; Pan, S.; Xu, X. A structure-activity relationship study of flavonoids as inhibitors of E. coli by membrane interaction effect. Biochim. Biophys. Acta 2013, 1828, 2751-2756.
81. Ajdzanović, V.; Spasojević, I.; Filipović, B.; Sosić-Jurjević, B.; Sekulić, M.; Milosević, V. Effects of genistein and daidzein on erythrocyte membrane fluidity: An electron paramagnetic resonance study. Can. J. Physiol. Pharmacol. 2010, 88, 497-500
82. Tsuchiya, H. Structure-dependent membrane interaction of flavonoids associated with their bioactivity. Food Chem. 2010, 120, 1089-1096.
83. Margina, D.; Ilie, M.; Manda, G.; Neagoe, I.; Mocanu, M.; Ionescu, D.; Gradinaru, D.; Ganea, C. Quercetin and epigallocatechin gallate effects on the cell membranes biophysical properties correlate with their antioxidant potential. Gen. Physiol. Biophys. 2012, 31, 47-55.
84. Alvarez-Suarez, J.M.; Giampieri, F.; González-Paramás, A.M.; Damiani, E.; Astolfi, P.; Martinez-Sanchez, G.; Bompadre, S.; Quiles, J.L.; Santos-Buelga, C.; Battino, M. Phenolics from monofloral honeys protect human erythrocyte membranes against oxidative damage. Food Chem. Toxicol. 2012, 50, 1508-1516.
85. Selvaraj, S.; Krishnaswamy, S.; Devashya, V.; Sethuraman, S.; Krishnan, U.M. Influence of membrane lipid composition on flavonoid-membrane interactions: Implications on their biological activity. Prog. Lipid Res. 2015, 58, 1-13.
86. Tsuchiya, H. Effects of green tea catechins on membrane fluidity. Pharmacology 1999, 59, 34-44.
87. Tsuchiya, H. Stereospecificity in membrane effects of catechins. Chem. Biol. Interact. 2001, 134, 41-54.
88. Tsuchiya, H.; Sato, M.; Kato, H.; Okubo, T.; Juneja, L.R.; Kim, M. Simultaneous determination of catechins in human saliva by high-performance liquid chromatography. J. Chromatogr. B 1998, 703, 253-258.
89. Cyboran, S.; Strugała, P.; Włoch, A.; Oszmiański, J.; Kleszczyńska, H. Concentrated green tea supplement: Biological activity and molecular mechanisms. Life Sci. 2015, 126, 1-9.
90. Bard, M.; Albrecht, M.R.; Gupta, N.; Guynn, C.J.; Stillwell, W. Geraniol interferes with membrane functions in strains of Candida and Saccharomyces. Lipids 1988, 23, 534-538.
91. Nowotarska, S.W.; Nowotarski, K.J.; Friedman, M.; Situ, C. Effect of structure on the interactions between five natural antimicrobial compounds and phospholipids of bacterial cell membrane on model monolayers. Molecules 2014, 19, 7497-7515.
92. Reiner, G.N.; Fraceto, L.F.; de Paula, E.; Perillo, M.A.; García, D.A. Effects of gabaergic phenols on phospholipid bilayers as evaluated by 1H-NMR. J. Biomater. Nanobiotechnol. 2013, 4, 28-34.
93. Reiner, G.N.; Delgado-Marín, L.; Olguín, N.; Sánchez-Redondo, S.; Sánchez-Borzone, M.; Rodríguez-Farré, E.; Suñol, C.; García, D.A. Gabaergic pharmacological activity of propofol related compounds as possible enhancers of general anesthetics and interaction with membranes. Cell Biochem. Biophys. 2013, 67, 515-525.
94. Mendanha, S.A.; Moura, S.S.; Anjos, J.L.; Valadares, M.C.; Alonso, A. Toxicity of terpenes on fibroblast cells compared to their hemolytic potential and increase in erythrocyte membrane fluidity. Toxicol. In Vitro 2013, 27, 323-329.
95. Zengin, H.; Baysal, A.H. Antibacterial and antioxidant activity of essential oil terpenes against pathogenic and spoilage-forming bacteria and cell structure-activity relationships evaluated by SEM microscopy. Molecules 2014, 19, 17773-17798.
96. Nomura, T.; Kurihara, K. Liposomes as a model for olfactory cells: Changes in membrane potential in response to various odorants. Biochemistry 1987, 26, 6135-6140.
97. Yin, Q.; Shi, X.; Ding, H.; Dai, X.; Wan, G.; Qiao, Y. Interactions of borneol with DPPC phospholipid membranes: A molecular dynamics simulation study. Int. J. Mol. Sci. 2014, 15, 20365-20381.
98. DeFeudis, F.V.; Drieu, K. Ginkgo biloba extract (EGb 761) and CNS functions: Basic studies and clinical applications. Curr. Drug Targets 2000, 1, 25-58.
99. Marín, L.D.; Sánchez-Borzone, M.; García, D.A. Comparative antioxidant properties of some GABAergic phenols and related compounds, determined for homogeneous and membrane systems. Med. Chem. 2011, 7, 317-324.
100. Camargos, H.S.; Moreira, R.A.; Mendanha, S.A.; Fernandes, K.S.; Dorta, M.L.; Alonso, A. Terpenes increase the lipid dynamics in the Leishmania plasma membrane at concentrations similar to their IC50 values. PLoS ONE 2014, 9, e104429.
101. Tsuchiya, H.; Nagayama, M.; Tanaka, T.; Furusawa, M.; Kashimata, M.; Takeuchi, H. Membrane-rigidifying effects of anti-cancer dietary factors. Biofactors 2002, 16, 45-56.
102. Selvaraj, S.; Mohan, A.; Narayanan, S.; Sethuraman, S.; Krishnan, U.M. Dose-dependent interaction of trans-resveratrol with biomembranes: Effects on antioxidant property. J. Med. Chem. 2013, 56, 970-981.
103. Brittes, J.; Lúcio, M.; Nunes, C.; Lima, J.L.; Reis, S. Effects of resveratrol on membrane biophysical properties: Relevance for its pharmacological effects. Chem. Phys. Lipids 2010, 163, 747-754.
104. Wesołowska, O.; Kuzdzał, M.; Štrancar, J.; Michalak, K. Interaction of the chemopreventive agent resveratrol and its metabolite, peceatannol, with model membranes. Biochim. Biophys. Acta 2009, 1788, 1851-1860.
105. Sun, D.; Hurdle, J.G.; Lee, R.; Lee, R.; Cushman, M.; Pezzuto, J.M. Evaluation of flavonoid and resveratrol chemical libraries reveals abyssinone II as a promising antibacterial lead. ChemMedChem 2012, 7, 1541-1545.
106. Meddings, J.B.; Hogaboam, C.M.; Tran, K.; Reynolds, J.D.; Wallace, J.L. Capsaicin effects on non-neuronal plasma membranes. Biochim. Biophys. Acta 1991, 1070, 43-50.
107. Tsuchiya, H. Biphasic membrane effects of capsaicin, an active component in Capsicum species. J. Ethnopharmacol. 2001, 75, 295-299.
108. Kempaiah, R.K.; Srinivasan, K. Influence of dietary spices on the fluidity of erythrocytes in hypercholesterolaemic rats. Br. J. Nutr. 2005, 93, 81-91.
109. Prakash, U.N.; Srinivasan, K. Beneficial influence of dietary spices on the ultrastructure and fluidity of the intestinal brush border in rats. Br. J. Nutr. 2010, 104, 31-39.
110. Binshtok, A.M.; Bean, B.P.; Woolf, C.J. Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature 2007, 449, 607-610.
111. Tsuchiya, H.; Mizogami, M. Plant components exhibit pharmacological activities and drug interactions by acting on lipid membranes. Pharmacogn. Commun. 2012, 2, 58-71.
112. Asgarpanah, J. Phytochemistry, pharmacology and medicinal properties of Hypericum perforatum L. Afr. J. Pharm. Pharmacol. 2012, 6, 1387-1394.
113. Eckert, G.P.; Müller, W.E. Effects of hyperforin on the fluidity of brain membranes. Pharmacopsychiatry 2001, 34, S22-S25.
114. Eckert, G.P.; Keller, J.H.; Jourdan, C.; Karas, M.; Volmer, D.A.; Schubert-Zsilavecz, M.; Müller, W.E. Hyperforin modifies neuronal membrane properties in vivo. Neurosci. Lett. 2004, 367, 139-143.
115. Chaloupka, R.; Obšil, T.; Plášek, J.; Sureau, F. The effect of hypericin and hypocrellin-A on lipid membranes and membrane potential of 3T3 fibroblasts. Biochim. Biophys. Acta 1999, 1418, 39-47.
116. Kraus, B.; Wolff, H.; Heilmann, J.; Elstner, E.F. Influence of Hypericum perforatum extract and its single compounds on amyloid-β mediated toxicity in microglial cells. Life Sci. 2007, 81, 884-894.
117. Tsuchiya, H.; Nagayama, M. Garlic allyl derivatives interact with membrane lipids to modify the membrane fluidity. J. Biomed. Sci. 2008, 15, 653-660.
118. Debouzy, J.C.; Neumann, J.M.; Hervé, M.; Daveloose, D.; Viret, J.; Apitz-Castro, R. Interaction of antiaggregant molecule ajoene with membranes. An ESR and 1H-, 2H-, 31P-NMR study. Eur. Biophys. J. 1989, 17, 211-216.
119. Rendu, F.; Daveloose, D.; Debouzy, J.C.; Bourdeau, N.; Levy-Toledano, S.; Jain, M.K.; Apitz-Castro, R. Ajoene, the antiplatelet compound derived from garlic, specifically inhibits platelet release reaction by affecting the plasma membrane internal microviscosity. Biochem. Pharmacol. 1989, 38, 1321-1328.
120. Knowles, L.M.; Milner, J.A. Allyl sulfides modify cell growth. Drug Metabol. Drug Interact. 2000, 17, 81-107.
121. Rosenkranz, V.; Wink, M. Alkaloids induce programmed cell death in bloodstream forms of trypanosomes (Trypanosoma b. brucei). Molecules 2008, 13, 2462-2473.
122. Moloudizargari, M.; Mikaili, P.; Aghajanshakeri, S.; Asghari, M.H.; Shayegh, J. Pharmacological and therapeutic effects of Peganum harmala and its main alkaloids. Pharmacogn. Rev. 2013, 7, 199-212.
123. Cao, R.; Peng, W.; Wang, Z.; Xu, A. β-Carboline alkaloids: Biochemical and pharmacological functions. Curr. Med. Chem. 2007, 14, 479-500.
124. Peura, P.; Mackenzie, P.; Koivusaari, U.; Lang, M. Increased fluidity of a model membrane caused by tetrahydro-β-carbolines. Mol. Pharmacol. 1982, 22, 721-724.
125. Tsuchiya, H.; Ohmoto, S. Comparative effects of β-carbolines on platelet aggregation and lipid membranes. Pharmacol. Rep. 2010, 62, 689-695.
126. Tsuchiya, H. Biphasic effects of acetaldehyde-biogenic amine condensation products on membrane fluidity. J. Pharm. Pharmacol. 2001, 53, 121-127.
127. Tsuchiya, H. Inhibition of membrane effects of general anesthetic propofol by benzodiazepine inverse agonist tetrahydro-β-carboline. Int. J. Pharmacol. 2012, 8, 542-548.
128. Tsuchiya, H.; Mizogami, M. Drinking-related tetrahydroharmans counteract the membrane effects of local anesthetic lidocaine. J. Drug Alcohol Res. 2014, 3, doi:10.4303/jdar/235887.
129. Budai, M.; Szabó, Z.; Szogyi, M.; Gróf, P. Molecular interactions between DPPC and morphine derivatives: A DSC and ESR study. Int. J. Pharm. 2003, 250, 239-250.
130. Khajuria, A.; Thusu, N.; Zutshi, U. Piperine modulates permeability characteristics of intestine by inducing alterations in membrane dynamics: Influence on brush border membrane fluidity, ultrastructure and enzyme kinetics. Phytomedicine 2002, 9, 224-231.
131. Gąsiorowska, J.; Wesołowska, O.; Michalak, K. Interaction of plant alkaloid, berberine, with zwitterionic and negatively charged phospholipid bilayers. Curr. Top. Biophys. 2011, 34, 45-51.
132. Alves, D.S.; Pérez-Fons, L.; Estepa, A.; Micol, V. Membrane-related effects underlying the biological activity of the anthraquinones emodin and barbaloin. Biochem. Pharmacol. 2004, 68, 549-561.
133. Duarte, E.L.; Oliveira, T.R.; Alves, D.S.; Micol, V.; Lamy, M.T. On the interaction of the anthraquinone barbaloin with negatively charged DMPG bilayers. Langmuir 2008, 24, 4041-4049.
134. Yi, J.S.; Choo, H.J.; Cho, B.R.; Kim, H.M.; Kim, Y.N.; Ham, Y.M.; Ko, Y.G. Ginsenoside Rh2 induces ligand-independent Fas activation via lipid raft disruption. Biochem. Biophys. Res. Commun. 2009, 385, 154-159.
135. Zhou, X.M.; Cao, Y.L.; Dou, D.Q. Protective effect of ginsenoside-Re against cerebral ischemia/reperfusion damage in rats. Biol. Pharm. Bull. 2006, 29, 2502-2505.
136. Kwon, H.Y.; Kim, E.H.; Kim, S.W.; Kim, S.N.; Park, J.D.; Rhee, D.K. Selective toxicity of ginsenoside Rg3 on multidrug resistant cells by membrane fluidity modulation. Arch. Pharm. Res. 2008, 31, 171-177.
137. Tachikawa, E.; Kudo, K.; Nunokawa, M.; Kashimoto, T.; Takahashi, E.; Kitagawa, S. Characterization of ginseng saponin ginsenoside-Rg3 inhibition of catecholamine secretion in bovine adrenal chromaffin cells. Biochem. Pharmacol. 2001, 62, 943-951.
138. Han, S.K.; Ko, Y.I.; Park, S.J.; Jin, I.J.; Kim, Y.M. Oleanolic acid and ursolic acid stabilize liposomal membranes. Lipids 1997, 32, 769-773.
139. Broniatowski, M.; Flasiński, M.; Zięba, K.; Mis̈kowiec, P. Interactions of pentacyclic triterpene acids with cardiolipins and related phosphatidylglycerols in model systems. Biochim. Biophys. Acta 2014, 1838, 2530-2538.
140. Jaruga, E.; Sokal, A.; Chrul, S.; Bartosz, G. Apoptosis-independent alterations in membrane dynamics induced by curcumin. Exp. Cell Res. 1998, 245, 303-312.
141. Atsumi, T.; Fujisawa, S.; Tonosaki, K. Relationship between intracellular ROS production and membrane mobility in curcumin- and tetrahydrocurcumin-treated human gingival fibroblasts and human submandibular gland carcinoma cells. Oral Dis. 2005, 11, 236-242.
142. Sun, Y.; Lee, C.C.; Hung, W.C.; Chen, F.Y.; Lee, M.T.; Huang, H.W. The bound states of amphipathic drugs in lipid bilayers: Study of curcumin. Biophys. J. 2008, 95, 2318-2324.
143. Hung, W.C.; Chen, F.Y.; Lee, C.C.; Sun, Y.; Lee, M.T.; Huang, H.W. Membrane-thinning effect of curcumin. Biophys. J. 2008, 94, 4331-4338.
144. Bohn, T. Dietary factors affecting polyphenol bioavailability. Nutr. Rev. 2014, 72, 429-452.
145. Ma, Y.; Zeng, M.; Sun, R.; Hu, M. Disposition of flavonoids impacts their efficacy and safety. Curr. Drug Metab. 2014, 15, 841-864.
146. Thilakarathna, S.H.; Rupasinghe, H.P. Flavonoid bioavailability and attempts for bioavailability enhancement. Nutrients 2013, 5, 3367-3387.
147. Murota, K.; Terao, J. Antioxidative flavonoid quercetin: Implication of its intestinal absorption and metabolism. Arch. Biochem. Biophys. 2003, 417, 12-17.
148. Goldberg, D.M.; Yan, J.; Soleas, G.J. Absorption of three wine-related polyphenols in three different matrices by healthy subjects. Clin. Biochem. 2003, 36, 79-87.
149. Oh, H.J.; Shin, K.C.; Oh, D.K. Production of ginsenosides Rg1 and Rh1 by hydrolyzing the outer glycoside at the C-6 position in protopanaxatriol-type ginsenosides using β-glucosidase from Pyrococcus furiosus. Biotechnol. Lett. 2014, 36, 113-119.
150. Shin, S.; Jang, J.Y.; Park, D.; Yon, J.M.; Baek, I.J.; Hwang, B.Y.; Nam, S.Y.; Yun, Y.W.; Kim, K.Y.; Joo, S.S.; et al. Korean red ginseng extract does not cause embryo-fetal death or abnormalities in mice. Birth Defects Res. B Dev. Reprod. Toxicol. 2010, 89, 78-85.
151. Han, M.; Fang, X.L. Difference in oral absorption of ginsenoside Rg1 between in vitro and in vivo models. Acta Pharmacol. Sin. 2006, 27, 499-505.
152. Kim, H.K. Pharmacokinetics of ginsenoside Rb1 and its metabolite compound K after oral administration of Korean Red Ginseng extract. J. Ginseng Res. 2013, 37, 451-456.
153. Ingólfsson, H.I.; Thakur, P.; Herold, K.F.; Hobart, E.A.; Ramsey, N.B.; Periole, X.; de Jong, D.H.; Zwama, M.; Yilmaz, D.; Hall, K.; et al. Phytochemicals perturb membranes and promiscuously alter protein function. ACS Chem. Biol. 2014, 9, 1788-1798.
154. Hendrich, A. Flavonoid-membrane interactions: Possible consequences for biological effects of some polyphenolic compounds. Acta Pharmacol. Sin. 2006, 27, 27-40.
155. Erlejman, A.G.; Verstraeten, S.V.; Fraga, C.G.; Oteiza, P.I. The interaction of flavonoids with membranes: Potential determinant of flavonoid antioxidant effects. Free Radic. Res. 2004, 38, 1311-1320.
156. Sinha, R.; Srivastava, S.; Joshi, A.; Joshi, U.J.; Govil, G. In-vitro anti-proliferative and anti-oxidant activity of galangin, fisetin and quercetin: Role of localization and intermolecular interaction in model membrane. Eur. J. Med. Chem. 2014, 79, 102-109.
157. Phan, H.T.; Yoda, T.; Chahal, B.; Morita, M.; Takagi, M.; Vestergaard, M.C. Structure-dependent interactions of polyphenols with a biomimetic membrane system. Biochim. Biophys. Acta 2014, 1838, 2670-2677.
158. Furusawa, M.; Tsuchiya, H.; Nagayama, M.; Tanaka, T.; Nakaya, K.; Iinuma, M. Anti-platelet and membrane-rigidifying flavonoids in brownish scale of onion. J. Health Sci. 2003, 49, 475-480.
159. Furusawa, M.; Tsuchiya, H.; Nagayama, M.; Tanaka, T.; Oyama, M.; Ito, T.; Iinuma, M.; Takeuchi, H. Cell growth inhibition by membrane-active components in brownish scale of onion. J. Health Sci. 2006, 52, 578-584.
160. Tsuchiya, H.; Tanaka, T.; Nagayama, M.; Oyama, M.; Iinuma, M. Membrane activity-guided isolation of antiproliferative and antiplatelet constituent from Evodiopanax innovans. Nat. Prod. Commun. 2008, 3, 809-814.
161. Oyedapo, O.O.; Akinpelu, B.A.; Akinwunmi, K.F.; Adeyinka, M.O.; Sipeolu, F.O. Red blood cell membrane stabilizing potentials of extracts of Lantana camara and its fractions. Int. J. Plant Physiol. Biochem. 2010, 2, 46-51.
162. Raimi, M.M.; Oyedapo, O.O. Bioactivity-guided evaluation of the root extract of Plumbago zeylanica. Int. J. Biol. Chem. Sci. 2009, 3, 672-680.
163. Gadamsetty, G.; Maru, S.; Tyagi, A.; Chakravarthula, S.N. Anti-inflammatory, cytotoxic and antioxidant effects of methanolic extracts of Drypetes Sepiaria (Euphorbiaceae). Afr. J. Tradit. Complement. Altern. Med. 2013, 10, 274-282.