Interaction of drugs with lipid raft membrane domains as a possible target
DOI:
https://doi.org/10.33393/dti.2020.2185Keywords:
Drug target, Fluidity, Lipid raft, Membrane domain, Membrane interactionAbstract
Introduction: Plasma membranes are not the homogeneous bilayers of uniformly distributed lipids but the lipid complex with laterally separated lipid raft membrane domains, which provide receptor, ion channel and enzyme proteins with a platform. The aim of this article is to review the mechanistic interaction of drugs with membrane lipid rafts and address the question whether drugs induce physicochemical changes in raft-constituting and raft-surrounding membranes.
Methods: Literature searches of PubMed/MEDLINE and Google Scholar databases from 2000 to 2020 were conducted to include articles published in English in internationally recognized journals. Collected articles were independently reviewed by title, abstract and text for relevance.
Results: The literature search indicated that pharmacologically diverse drugs interact with raft model membranes and cellular membrane lipid rafts. They could physicochemically modify functional protein-localizing membrane lipid rafts and the membranes surrounding such domains, affecting the raft organizational integrity with the resultant exhibition of pharmacological activity. Raft-acting drugs were characterized as ones to decrease membrane fluidity, induce liquid-ordered phase or order plasma membranes, leading to lipid raft formation; and ones to increase membrane fluidity, induce liquid-disordered phase or reduce phase transition temperature, leading to lipid raft disruption.
Conclusion: Targeting lipid raft membrane domains would open a new way for drug design and development. Since angiotensin-converting enzyme 2 receptors which are a cell-specific target of and responsible for the cellular entry of novel coronavirus are localized in lipid rafts, agents that specifically disrupt the relevant rafts may be a drug against coronavirus disease 2019.
Downloads
References
Kusumi A, Fujiwara TK, Chadda R, et al. Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson’s fluid-mosaic model. Annu Rev Cell Dev Biol. 2012;28(1):215-250. https://doi.org/10.1146/annurev-cellbio-100809-151736 PMID:22905956
Pike LJ. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J Lipid Res. 2006;47(7):1597-1598. https://doi.org/10.1194/jlr.E600002-JLR200 PMID:16645198
Hanzal-Bayer MF, Hancock JF. Lipid rafts and membrane traffic. FEBS Lett. 2007;581(11):2098-2104. https://doi.org/10.1016/j.febslet.2007.03.019 PMID:17382322
McMullen T, Lewis R, McElhany R. Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes. Curr Opin Colloid Interface Sci. 2004;8(6):459-468. https://doi.org/10.1016/j.cocis.2004.01.007
Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000;1(1):31-39. https://doi.org/10.1038/35036052 PMID:11413487
Laude AJ, Prior IA. Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol. 2004;21(3):193-205. https://doi.org/10.1080/09687680410001700517PMID:15204627
George KS, Wu S. Lipid raft: A floating island of death or survival. Toxicol Appl Pharmacol. 2012;259(3):311-319. https://doi.org/10.1016/j.taap.2012.01.007 PMID:22289360
O’Connell KM, Martens JR, Tamkun MM. Localization of ion channels to lipid Raft domains within the cardiovascular system. Trends Cardiovasc Med. 2004;14(2):37-42. https://doi.org/10.1016/j.tcm.2003.10.002 PMID:15030787
Maguy A, Hebert TE, Nattel S. Involvement of lipid rafts and caveolae in cardiac ion channel function. Cardiovasc Res. 2006;69(4):798-807. https://doi.org/10.1016/j.cardiores.2005.11.013PMID:16405931
Dalskov SM, Immerdal L, Niels-Christiansen LL, Hansen GH, Schousboe A, Danielsen EM. Lipid raft localization of GABA A receptor and Na+, K+-ATPase in discrete microdomain clusters in rat cerebellar granule cells. Neurochem Int. 2005;46(6):489-499. https://doi.org/10.1016/j.neuint.2004.11.010 PMID:15769551
Patel HH, Murray F, Insel PA. G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains. Handb Exp Pharmacol. 2008;186(186):167-184. https://doi.org/10.1007/978-3-540-72843-6_7 PMID:18491052
Xiang Y, Rybin VO, Steinberg SF, Kobilka B. Caveolar localization dictates physiologic signaling of β 2-adrenoceptors in neonatal cardiac myocytes. J Biol Chem. 2002;277(37):34280-34286. https://doi.org/10.1074/jbc.M201644200 PMID:12097322
Pottosin II, Valencia-Cruz G, Bonales-Alatorre E, Shabala SN, Dobrovinskaya OR. Methyl-β-cyclodextrin reversibly alters the gating of lipid rafts-associated Kv1.3 channels in Jurkat T lymphocytes. Pflugers Arch. 2007;454(2):235-244. https://doi.org/10.1007/s00424-007-0208-4PMID:17242956
Levitt ES, Clark MJ, Jenkins PM, Martens JR, Traynor JR. Differential effect of membrane cholesterol removal on μ- and δ-opioid receptors: a parallel comparison of acute and chronic signaling to adenylyl cyclase. J Biol Chem. 2009;284(33):22108-22122. https://doi.org/10.1074/jbc.M109.030411 PMID:19520863
Ding XQ, Fitzgerald JB, Matveev AV, McClellan ME, Elliott MH. Functional activity of photoreceptor cyclic nucleotide-gated channels is dependent on the integrity of cholesterol- and sphingolipid-enriched membrane domains. Biochemistry. 2008;47(12):3677-3687. https://doi.org/10.1021/bi7019645 PMID:18303857
Gandhavadi M, Allende D, Vidal A, Simon SA, McIntosh TJ. Structure, composition, and peptide binding properties of detergent soluble bilayers and detergent resistant rafts. Biophys J. 2002;82(3):1469-1482. https://doi.org/10.1016/S0006-3495(02)75501-X PMID:11867462
Koumanov KS, Tessier C, Momchilova AB, Rainteau D, Wolf C, Quinn PJ. Comparative lipid analysis and structure of detergent-resistant membrane raft fractions isolated from human and ruminant erythrocytes. Arch Biochem Biophys. 2005;434(1):150-158. https://doi.org/10.1016/j.abb.2004.10.025 PMID:15629118
Holland GP, McIntyre SK, Alam TM. Distinguishing individual lipid headgroup mobility and phase transitions in raft-forming lipid mixtures with 31P MAS NMR. Biophys J. 2006;90(11):4248-4260. https://doi.org/10.1529/biophysj.105.077289 PMID:16533851
Simons K, Ehehalt R. Cholesterol, lipid rafts, and disease. J Clin Invest. 2002;110(5):597-603. https://doi.org/10.1172/JCI0216390 PMID:12208858
Jacobson K, Mouritsen OG, Anderson RG. Lipid rafts: at a crossroad between cell biology and physics. Nat Cell Biol. 2007;9(1):7-14. https://doi.org/10.1038/ncb0107-7 PMID:17199125
Boesze-Battaglia K. Isolation of membrane rafts and signaling complexes. Methods Mol Biol. 2006;332:169-179. https://doi.org/10.1385/1-59745-048-0:167 PMID:16878692
Loftsson T, Magnúsdóttir A, Másson M, Sigurjónsdóttir JF. Self-association and cyclodextrin solubilization of drugs. J Pharm Sci. 2002;91(11):2307-2316. https://doi.org/10.1002/jps.10226PMID:12379916
Mahammad S, Parmryd I. Cholesterol depletion using methyl-β-cyclodextrin. Methods Mol Biol. 2015;1232:91-102. https://doi.org/10.1007/978-1-4939-1752-5_8 PMID:25331130
Chau PL. New insights into the molecular mechanisms of general anaesthetics. Br J Pharmacol. 2010;161(2):288-307. https://doi.org/10.1111/j.1476-5381.2010.00891.x PMID:20735416
Olsen RW, Li GD. GABA(A) receptors as molecular targets of general anesthetics: identification of binding sites provides clues to allosteric modulation. Can J Anaesth. 2011;58(2):206-215. https://doi.org/10.1007/s12630-010-9429-7 PMID:21194017
Yamakura T, Harris RA. Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels. Comparison with isoflurane and ethanol. Anesthesiology. 2000;93(4):1095-1101. https://doi.org/10.1097/00000542-200010000-00034 PMID:11020766
Daniell LC. Effect of anesthetic and convulsant barbiturates on N-methyl-D-aspartate receptor-mediated calcium flux in brain membrane vesicles. Pharmacology. 1994;49(5):296-307. https://doi.org/10.1159/000139246 PMID:7862741
Li X, Serwanski DR, Miralles CP, Bahr BA, De Blas AL. Two pools of Triton X-100-insoluble GABA(A) receptors are present in the brain, one associated to lipid rafts and another one to the post-synaptic GABAergic complex. J Neurochem. 2007;102(4):1329-1345. https://doi.org/10.1111/j.1471-4159.2007.04635.x PMID:17663755
Parat MO. Could endothelial caveolae be the target of general anaesthetics? Br J Anaesth. 2006;96(5):547-550. https://doi.org/10.1093/bja/ael079 PMID:16600902
Tsuchiya H. Structure-specific membrane-fluidizing effect of propofol. Clin Exp Pharmacol Physiol. 2001;28(4):292-299. https://doi.org/10.1046/j.1440-1681.2001.03441.x PMID:11251643
Tsuchiya H, Ueno T, Tanaka T, Matsuura N, Mizogami M. Comparative study on determination of antioxidant and membrane activities of propofol and its related compounds. Eur J Pharm Sci. 2010;39(1-3):97-102. https://doi.org/10.1016/j.ejps.2009.11.001 PMID:19897032
Gray E, Karslake J, Machta BB, Veatch SL. Liquid general anesthetics lower critical temperatures in plasma membrane vesicles. Biophys J. 2013;105(12):2751-2759. https://doi.org/10.1016/j.bpj.2013.11.005 PMID:24359747
Grim KJ, Abcejo AJ, Barnes A, et al. Caveolae and propofol effects on airway smooth muscle. Br J Anaesth. 2012;109(3):444-453. https://doi.org/10.1093/bja/aes130 PMID:22542538
Patel J, Chowdhury EA, Noorani B, Bickel U, Huang J. Isoflurane increases cell membrane fluidity significantly at clinical concentrations. Biochim Biophys Acta Biomembr. 2020;1862(2):183140. https://doi.org/10.1016/j.bbamem.2019.183140 PMID:31790694
Turkyilmaz S, Almeida PF, Regen SL. Effects of isoflurane, halothane, and chloroform on the interactions and lateral organization of lipids in the liquid-ordered phase. Langmuir. 2011;27(23):14380-14385. https://doi.org/10.1021/la2035278 PMID:21995557
Weinrich M, Nanda H, Worcester DL, Majkrzak CF, Maranville BB, Bezrukov SM. Halothane changes the domain structure of a binary lipid membrane. Langmuir. 2012;28(10):4723-4728. https://doi.org/10.1021/la204317k PMID:22352350
Weinrich M, Worcester DL. Xenon and other volatile anesthetics change domain structure in model lipid raft membranes. J Phys Chem B. 2013;117(50):16141-16147. https://doi.org/10.1021/jp411261g PMID:24299622
Sierra-Valdez FJ, Ruiz-Suárez JC, Delint-Ramirez I. Pentobarbital modifies the lipid raft-protein interaction: A first clue about the anesthesia mechanism on NMDA and GABAA receptors. Biochim Biophys Acta. 2016;1858(11):2603-2610. https://doi.org/10.1016/j.bbamem.2016.07.011PMID:27457704
Fozzard HA, Lee PJ, Lipkind GM. Mechanism of local anesthetic drug action on voltage-gated sodium channels. Curr Pharm Des. 2005;11(21):2671-2686. https://doi.org/10.2174/1381612054546833 PMID:16101448
Pristerá A, Okuse K. Building excitable membranes: lipid rafts and multiple controls on trafficking of electrogenic molecules. Neuroscientist. 2012;18(1):70-81. https://doi.org/10.1177/1073858410393977 PMID:21518816
Bao L. Trafficking regulates the subcellular distribution of voltage-gated sodium channels in primary sensory neurons. Mol Pain. 2015;11:61. https://doi.org/10.1186/s12990-015-0065-7PMID:26423360
Pristerà A, Baker MD, Okuse K. Association between tetrodotoxin resistant channels and lipid rafts regulates sensory neuron excitability. PLoS One. 2012;7(8):e40079. https://doi.org/10.1371/journal.pone.0040079 PMID:22870192
Kamata K, Manno S, Ozaki M, Takakuwa Y. Functional evidence for presence of lipid rafts in erythrocyte membranes: gsalpha in rafts is essential for signal transduction. Am J Hematol. 2008;83(5):371-375. https://doi.org/10.1002/ajh.21126 PMID:18181202
Bandeiras C, Serro AP, Luzyanin K, Fernandes A, Saramago B. Anesthetics interacting with lipid rafts. Eur J Pharm Sci. 2013;48(1-2):153-165. https://doi.org/10.1016/j.ejps.2012.10.023PMID:23142844
Yoshida K, Takashima A, Nishio I. Effect of dibucaine hydrochloride on raft-like lipid domains in model membrane system. MedChemComm. 2015;6(8):1444-1451. https://doi.org/10.1039/C5MD00108K
Sugahara K, Shimokawa N, Takagi M. Thermal stability of phase-separated domains in multicomponent lipid membranes with local anesthetics. Membranes (Basel). 2017;7(3):33. https://doi.org/10.3390/membranes7030033 PMID:28661445
Kinoshita M, Chitose T, Matsumori N. Mechanism of local anesthetic-induced disruption of raft-like ordered membrane domains. Biochim Biophys Acta, Gen Subj. 2019;1863(9):1381-1389. https://doi.org/10.1016/j.bbagen.2019.06.008 PMID:31207252
Groban L, Deal DD, Vernon JC, James RL, Butterworth J. Cardiac resuscitation after incremental overdosage with lidocaine, bupivacaine, levobupivacaine, and ropivacaine in anesthetized dogs. Anesth Analg. 2001;92(1):37-43. https://doi.org/10.1097/00000539-200101000-00008 PMID:11133597
Tsuchiya H, Ueno T, Mizogami M, Takakura K. Do local anesthetics interact preferentially with membrane lipid rafts? Comparative interactivities with raft-like membranes. J Anesth. 2010;24(4):639-642. https://doi.org/10.1007/s00540-010-0943-0 PMID:20414686
Tsuchiya H, Mizogami M. R(+)-, Rac-, and S(-)-bupivacaine stereostructure-specifically interact with membrane lipids at cardiotoxically relevant concentrations. Anesth Analg. 2012;114(2):310-312. https://doi.org/10.1213/ANE.0b013e31823ed410 PMID:22156330
Pontier SM, Percherancier Y, Galandrin S, Breit A, Galés C, Bouvier M. Cholesterol-dependent separation of the β2-adrenergic receptor from its partners determines signaling efficacy: insight into nanoscale organization of signal transduction. J Biol Chem. 2008;283(36):24659-24672. https://doi.org/10.1074/jbc.M800778200 PMID:18566454
Mizogami M, Takakura K, Tsuchiya H. The interactivities with lipid membranes differentially characterize selective and nonselective β1-blockers. Eur J Anaesthesiol. 2010;27(9):829-834. https://doi.org/10.1097/EJA.0b013e32833bf5e4 PMID:20601889
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;4:150. https://doi.org/10.3389/fphar.2013.00150 PMID:24339816
Prichard BN, Cruickshank JM, Graham BR. Beta-adrenergic blocking drugs in the treatment of hypertension. Blood Press. 2001;10(5-6):366-386. https://doi.org/10.1080/080370501753400665PMID:11822540
Callera GE, Montezano AC, Yogi A, Tostes RC, Touyz RM. Vascular signaling through cholesterol-rich domains: implications in hypertension. Curr Opin Nephrol Hypertens. 2007;16(2):90-104. https://doi.org/10.1097/MNH.0b013e328040bfbd PMID:17293683
Mizogami M, Tsuchiya H. Membrane interactivity of anesthetic adjuvant dexmedetomidine discriminable from clonidine and enantiomeric levomedetomidine. J Adv Med Med Res. 2019;29:1-15. https://doi.org/10.9734/jammr/2019/v29i1130142
Morris DP, Lei B, Wu YX, Michelotti GA, Schwinn DA. The α1a-adrenergic receptor occupies membrane rafts with its G protein effectors but internalizes via clathrin-coated pits. J Biol Chem. 2008;283(5):2973-2985. https://doi.org/10.1074/jbc.M705795200 PMID:18048357
Huang P, Xu W, Yoon SI, et al. Agonist treatment did not affect association of mu opioid receptors with lipid rafts and cholesterol reduction had opposite effects on the receptor-mediated signaling in rat brain and CHO cells. Brain Res. 2007;1184:46-56. https://doi.org/10.1016/j.brainres.2007.09.096 PMID:17980352
Heron DS, Shinitzky M, Zamir N, Samuel D. Adaptive modulations of brain membrane lipid fluidity in drug addiction and denervation supersensitivity. Biochem Pharmacol. 1982;31(14):2435-2438. https://doi.org/10.1016/0006-2952(82)90543-3 PMID:6889866
Budai M, Szabó Z, Szogyi M, Gróf P. Molecular interactions between DPPC and morphine derivatives: a DSC and EPR study. Int J Pharm. 2003;250:239–250. https://doi.org/10.1016/s0378-5173(02)00560-4. https://doi.org/10.1016/S0378-5173(02)00560-4
Zheng H, Chu J, Qiu Y, Loh HH, Law PY. Agonist-selective signaling is determined by the receptor location within the membrane domains. Proc Natl Acad Sci USA. 2008;105(27):9421-9426. https://doi.org/10.1073/pnas.0802253105 PMID:18599439
Liou JY, Deng WG, Gilroy DW, Shyue SK, Wu KK. Colocalization and interaction of cyclooxygenase-2 with caveolin-1 in human fibroblasts. J Biol Chem. 2001;276(37):34975-34982. https://doi.org/10.1074/jbc.M105946200 PMID:11432874
Alsop RJ, Toppozini L, Marquardt D, Kučerka N, Harroun TA, Rheinstädter MC. Aspirin inhibits formation of cholesterol rafts in fluid lipid membranes. Biochim Biophys Acta. 2015;1848(3):805-812. https://doi.org/10.1016/j.bbamem.2014.11.023 PMID:25475646
Alsop RJ, Himbert S, Dhaliwal A, Schmalzl K, Rheinstädter MC. Aspirin locally disrupts the liquid-ordered phase. R Soc Open Sci. 2018;5(2):171710. https://doi.org/10.1098/rsos.171710PMID:29515878
Zhou Y, Cho KJ, Plowman SJ, Hancock JF. Nonsteroidal anti-inflammatory drugs alter the spatiotemporal organization of Ras proteins on the plasma membrane. J Biol Chem. 2012;287(20):16586-16595. https://doi.org/10.1074/jbc.M112.348490 PMID:22433858
Alves ACS, Dias RA, Kagami LP, et al. Beyond the “lock and key” paradigm: targeting lipid rafts to induce the selective apoptosis of cancer cells. Curr Med Chem. 2018;25(18):2082-2104. https://doi.org/10.2174/0929867325666180111100601 PMID:29332565
van der Luit AH, Vink SR, Klarenbeek JB, et al. A new class of anticancer alkylphospholipids uses lipid rafts as membrane gateways to induce apoptosis in lymphoma cells. Mol Cancer Ther. 2007;6(8):2337-2345. https://doi.org/10.1158/1535-7163.MCT-07-0202 PMID:17699729
Alves AC, Ribeiro D, Nunes C, Reis S. Biophysics in cancer: the relevance of drug-membrane interaction studies. Biochim Biophys Acta. 2016;1858(9):2231-2244. https://doi.org/10.1016/j.bbamem.2016.06.025 PMID:27368477
Ausili A, Torrecillas A, Aranda FJ, et al. Edelfosine is incorporated into rafts and alters their organization. J Phys Chem B. 2008;112(37):11643-11654. https://doi.org/10.1021/jp802165nPMID:18712919
Gomide AB, Thomé CH, dos Santos GA, et al. Disrupting membrane raft domains by alkylphospholipids. Biochim Biophys Acta. 2013;1828(5):1384-1389. https://doi.org/10.1016/j.bbamem.2013.01.017 PMID:23376656
Castro BM, Fedorov A, Hornillos V, et al. Edelfosine and miltefosine effects on lipid raft properties: membrane biophysics in cell death by antitumor lipids. J Phys Chem B. 2013;117(26):7929-7940. https://doi.org/10.1021/jp401407d PMID:23738749
Wnętrzak A, Łątka K, Makyła-Juzak K, Zemla J, Dynarowicz-Łątka P. The influence of an antitumor lipid - erucylphosphocholine - on artificial lipid raft system modeled as Langmuir monolayer. Mol Membr Biol. 2015;32(5-8):189-197. https://doi.org/10.3109/09687688.2015.1125537 PMID:26911703
Węder K, Mach M, Hąc-Wydro K, Wydro P. Studies on the interactions of anticancer drug - Minerval - with membrane lipids in binary and ternary Langmuir monolayers. Biochim Biophys Acta Biomembr. 2018;1860(11):2329-2336. https://doi.org/10.1016/j.bbamem.2018.05.019 PMID:29864405
Rebillard A, Lagadic-Gossmann D, Dimanche-Boitrel MT. Cisplatin cytotoxicity: DNA and plasma membrane targets. Curr Med Chem. 2008;15(26):2656-2663. https://doi.org/10.2174/092986708786242903 PMID:18991628
Lacour S, Hammann A, Grazide S, et al. Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer Res. 2004;64(10):3593-3598. https://doi.org/10.1158/0008-5472.CAN-03-2787 PMID:15150117
Rebillard A, Tekpli X, Meurette O, et al. Cisplatin-induced apoptosis involves membrane fluidification via inhibition of NHE1 in human colon cancer cells. Cancer Res. 2007;67(16):7865-7874. https://doi.org/10.1158/0008-5472.CAN-07-0353 PMID:17699793
Berquand A, Fa N, Dufrêne YF, Mingeot-Leclercq MP. Interaction of the macrolide antibiotic azithromycin with lipid bilayers: effect on membrane organization, fluidity, and permeability. Pharm Res. 2005;22(3):465-475. https://doi.org/10.1007/s11095-004-1885-8 PMID:15835753
Alves AC, Ribeiro D, Horta M, Lima JLFC, Nunes C, Reis S. A biophysical approach to daunorubicin interaction with model membranes: relevance for the drug’s biological activity. J R Soc Interface. 2017;14(133):20170408. https://doi.org/10.1098/rsif.2017.0408 PMID:28855387
Alves AC, Magarkar A, Horta M, et al. Influence of doxorubicin on model cell membrane properties: insights from in vitro and in silico studies. Sci Rep. 2017;7(1):6343. https://doi.org/10.1038/s41598-017-06445-z PMID:28740256
Tsuchiya H. Membrane interactions of phytochemicals as their molecular mechanism applicable to the discovery of drug leads from plants. Molecules. 2015;20(10):18923-18966. https://doi.org/10.3390/molecules201018923 PMID:26501254
1Tarahovsky YS, Kim YA, Yagolnik EA, Muzafarov EN. Flavonoid-membrane interactions: involvement of flavonoid-metal complexes in raft signaling. Biochim Biophys Acta. 2014;1838(5):1235-1246. https://doi.org/10.1016/j.bbamem.2014.01.021 PMID:24472512
Selvaraj S, Krishnaswamy S, Devashya V, Sethuraman S, Krishnan UM. Influence of membrane lipid composition on flavonoid-membrane interactions: implications on their biological activity. Prog Lipid Res. 2015;58:1-13. https://doi.org/10.1016/j.plipres.2014.11.002PMID:25479162
Tarahovsky YS, Muzafarov EN, Kim YA. Rafts making and rafts braking: how plant flavonoids may control membrane heterogeneity. Mol Cell Biochem. 2008;314(1-2):65-71. https://doi.org/10.1007/s11010-008-9766-9 PMID:18414995
Tsuchiya H, Mizogami M. Plant components exhibit pharmacological activities and drug interactions by acting on lipid membranes. Pharmacog Commun. 2012;2:58–71. https://doi.org/10.5530/pc.2012.4.9. http://phcogfirst.com/article/869
Psahoulia FH, Drosopoulos KG, Doubravska L, Andera L, Pintzas A. Quercetin enhances TRAIL-mediated apoptosis in colon cancer cells by inducing the accumulation of death receptors in lipid rafts. Mol Cancer Ther. 2007;6(9):2591-2599. https://doi.org/10.1158/1535-7163.MCT-07-0001 PMID:17876056
Kaneko M, Takimoto H, Sugiyama T, Seki Y, Kawaguchi K, Kumazawa Y. Suppressive effects of the flavonoids quercetin and luteolin on the accumulation of lipid rafts after signal transduction via receptors. Immunopharmacol Immunotoxicol. 2008;30(4):867-882. https://doi.org/10.1080/08923970802135690 PMID:18720166
Ionescu D, Margină D, Ilie M, Iftime A, Ganea C. Quercetin and epigallocatechin-3-gallate effect on the anisotropy of model membranes with cholesterol. Food Chem Toxicol. 2013;61:94-100. https://doi.org/10.1016/j.fct.2013.03.007 PMID:23523830
Tsuchiya H. Stereospecificity in membrane effects of catechins. Chem Biol Interact. 2001;134(1):41-54. https://doi.org/10.1016/S0009-2797(00)00308-2 PMID:11248221
Adachi S, Nagao T, Ingolfsson HI, et al. The inhibitory effect of (-)-epigallocatechin gallate on activation of the epidermal growth factor receptor is associated with altered lipid order in HT29 colon cancer cells. Cancer Res. 2007;67(13):6493-6501. https://doi.org/10.1158/0008-5472.CAN-07-0411 PMID:17616711
Duhon D, Bigelow RL, Coleman DT, et al. The polyphenol epigallocatechin-3-gallate affects lipid rafts to block activation of the c-Met receptor in prostate cancer cells. Mol Carcinog. 2010;49(8):739-749. https://doi.org/10.1002/mc.20649 PMID:20623641
Tsukamoto S, Hirotsu K, Kumazoe M, et al. Green tea polyphenol EGCG induces lipid-raft clustering and apoptotic cell death by activating protein kinase Cδ and acid sphingomyelinase through a 67 kDa laminin receptor in multiple myeloma cells. Biochem J. 2012;443(2):525-534. https://doi.org/10.1042/BJ20111837 PMID:22257159
Verstraeten SV, Oteiza PI, Fraga CG. Membrane effects of cocoa procyanidins in liposomes and Jurkat T cells. Biol Res. 2004;37(2):293-300. https://doi.org/10.4067/S0716-97602004000200016 PMID:15455659
Verstraeten SV, Jaggers GK, Fraga CG, Oteiza PI. Procyanidins can interact with Caco-2 cell membrane lipid rafts: involvement of cholesterol. Biochim Biophys Acta. 2013;1828(11):2646-2653. https://doi.org/10.1016/j.bbamem.2013.07.023 PMID:23899501
Neves AR, Nunes C, Reis S. Resveratrol induces ordered domains formation in biomembranes: implication for its pleiotropic action. Biochim Biophys Acta. 2016;1858(1):12-18. https://doi.org/10.1016/j.bbamem.2015.10.005 PMID:26456556
Alves DS, Pérez-Fons L, Estepa A, Micol V. Membrane-related effects underlying the biological activity of the anthraquinones emodin and barbaloin. Biochem Pharmacol. 2004;68(3):549-561. https://doi.org/10.1016/j.bcp.2004.04.012 PMID:15242821
Meng G, Liu Y, Lou C, Yang H. Emodin suppresses lipopolysaccharide-induced pro-inflammatory responses and NF-κB activation by disrupting lipid rafts in CD14-negative endothelial cells. Br J Pharmacol. 2010;161(7):1628-1644. https://doi.org/10.1111/j.1476-5381.2010.00993.x PMID:20726986
Huang Q, Shen HM, Shui G, Wenk MR, Ong CN. Emodin inhibits tumor cell adhesion through disruption of the membrane lipid Raft-associated integrin signaling pathway. Cancer Res. 2006;66(11):5807-5815. https://doi.org/10.1158/0008-5472.CAN-06-0077 PMID:16740720
Yi JS, Choo HJ, Cho BR, et al. Ginsenoside Rh2 induces ligand-independent Fas activation via lipid raft disruption. Biochem Biophys Res Commun. 2009;385(2):154-159. https://doi.org/10.1016/j.bbrc.2009.05.028 PMID:19445898
Wei Z, Wang J, Shi M, Liu W, Yang Z, Fu Y. Saikosaponin a inhibits LPS-induced inflammatory response by inducing liver X receptor alpha activation in primary mouse macrophages. Oncotarget. 2016;7(31):48995-49007. https://doi.org/10.18632/oncotarget.9863PMID:27285988
Murai T. The role of lipid rafts in cancer cell adhesion and migration. Int J Cell Biol. 2012;2012:763283. https://doi.org/10.1155/2012/763283 PMID:22253629
Li YC, Park MJ, Ye SK, Kim CW, Kim YN. Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents. Am J Pathol. 2006;168(4):1107-1118. https://doi.org/10.2353/ajpath.2006.050959 PMID:16565487
Zhang H, Penninger JM, Li Y, Zhong N, Slutsky AS. Angiotensin-converting enzyme 2 (ACE2) as a SARS-CoV-2 receptor: molecular mechanisms and potential therapeutic target. Intensive Care Med. 2020;46(4):586-590. https://doi.org/10.1007/s00134-020-05985-9 PMID:32125455
Lu Y, Liu DX, Tam JP. Lipid rafts are involved in SARS-CoV entry into Vero E6 cells. Biochem Biophys Res Commun. 2008;369(2):344-349. https://doi.org/10.1016/j.bbrc.2008.02.023 PMID:18279660
Glende J, Schwegmann-Wessels C, Al-Falah M, et al. Importance of cholesterol-rich membrane microdomains in the interaction of the S protein of SARS-coronavirus with the cellular receptor angiotensin-converting enzyme 2. Virology. 2008;381(2):215-221. https://doi.org/10.1016/j.virol.2008.08.026 PMID:18814896
Wang H, Yuan Z, Pavel MA, Hobson R, Hansen SB. The role of high cholesterol in age-related COVID19 lethality. bioRxiv. 2020.05.09.086249. https://doi.org/10.1101/2020.05.09.086249. https://doi.org/10.1101/2020.05.09.086249
Published
How to Cite
Issue
Section
Accepted 2020-11-11
Published 2020-12-22
