[en] Budesonide (BUD), a poorly soluble anti-inflammatory drug, is used to treat patients suffering from asthma and COPD (Chronic Obstructive Pulmonary Disease). Hydroxypropyl-β-cyclodextrin (HPβCD), a biocompatible cyclodextrin known to interact with cholesterol, is used as a drug-solubilizing agent in pharmaceutical formulations. Budesonide administered as an inclusion complex within HPβCD (BUD:HPβCD) required a quarter of the nominal dose of the suspension formulation and significantly reduced neutrophil induced inflammation in a COPD mouse model exceeding the effect of each molecule administered individually. This suggests the role of lipid domains enriched in cholesterol for inflammatory signaling activation.
In this context, we investigated the effect of BUD:HPβCD on the biophysical properties of membrane lipids. On cellular models (A549, lung epithelial cells), BUD:HPβCD extracted cholesterol similarly to HPβCD. On large unilamellar vesicles (LUVs), by using the fluorescent probes diphenylhexatriene (DPH) and calcein, we demonstrated an increase in membrane fluidity and permeability induced by BUD:HPβCD in vesicles containing cholesterol. On giant unilamellar vesicles (GUVs) and lipid monolayers, BUD:HPβCD induced the disruption of cholesterol-enriched raft-like liquid ordered domains as well as changes in lipid packing and lipid desorption from the cholesterol monolayers, respectively. Except for membrane fluidity, all these effects were enhanced when HPβCD was complexed with budesonide as compared with HPβCD. Since cholesterol-enriched domains have been linked to membrane signaling including pathways involved in inflammation processes, we hypothesized the effects of BUD:HPβCD could be partly mediated by changes in the biophysical properties of cholesterol-enriched domains.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
dos Santos, Andreia
Bayiha, Jules
Dufour, Gilles
Cataldo, Didier ; Université de Liège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Evrard, Brigitte ; Université de Liège > Département de pharmacie > Pharmacie galénique
Silva, Liana C
Deleu, Magali ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie des agro-biosystèmes
Mingeot-Leclercq, Marie-Paule
Language :
English
Title :
Changes in biophysical membrane properties induced by the Budesonide/ Hydroxy-β-cyclodextrin complex
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Bibliography
Singer, S.J., Nicolson, G.L., The fluid mosaic model of the structure of cell membranes. Science 175 (1972), 720–731.
van Meer, G., Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5 (1989), 247–275.
Simons, K., Ikonen, E., Functional rafts in cell membranes. Nature 387 (1997), 569–572.
Nicolson, G.L., The fluid-mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim. Biophys. Acta 2014 (1838), 1451–1466.
Goni, F.M., The basic structure and dynamics of cell membranes: an update of the Singer-Nicolson model. Biochim. Biophys. Acta 2014 (1838), 1467–1476.
Schroeder, R., London, E., Brown, D., Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 12130–12134.
Nickels, J.D., Cheng, X., Mostofian, B., Stanley, C., Lindner, B., Heberle, F.A., Perticaroli, S., Feygenson, M., Egami, T., Standaert, R.F., et al. Mechanical properties of nanoscopic lipid domains. J. Am. Chem. Soc. 137 (2015), 15772–15780.
Besenicar, M.P., Bavdek, A., Kladnik, A., Macek, P., Anderluh, G., Kinetics of cholesterol extraction from lipid membranes by methyl-beta-cyclodextrin—a surface plasmon resonance approach. Biochim. Biophys. Acta 2008 (1778), 175–184.
Murai, T., Lipid raft-mediated regulation of hyaluronan-CD44 interactions in inflammation and cancer. Front. Immunol. 6 (2015), 1–9.
Varshney, P., Yadav, V., Saini, N., Lipid rafts in immune signaling: current progress and future perspective. Immunology 149 (2016), 13–24.
Loftsson, T., Brewster, M.E., Pharmaceutical applications of cyclodextrins: basic science and product development. J. Pharm. Pharmacol. 62 (2010), 1607–1621.
Jambhekar, S.S., Breen, P., Cyclodextrins in pharmaceutical formulations I: structure and physicochemical properties, formation of complexes, and types of complex. Drug Discov. Today 21 (2016), 356–362.
Valente, A.J., Soderman, O., The formation of host-guest complexes between surfactants and cyclodextrins. Adv. Colloid Interf. Sci. 205 (2014), 156–176.
Wei, H., Yu, C.Y., Cyclodextrin-functionalized polymers as drug carriers for cancer therapy. Biomater. Sci. 3 (2015), 1050–1060.
Dufour, G., Bigazzi, W., Wong, N., Boschini, F., de Tullio, P., Piel, G., Cataldo, D., Evrard, B., Interest of cyclodextrins in spray-dried microparticles formulation for sustained pulmonary delivery of budesonide. Int. J. Pharm. 495 (2015), 869–878.
Hodgson, D., Mortimer, K., Harrison, T., Budesonide/formoterol in the treatment of asthma. Expert Rev. Respir. Med. 4 (2010), 557–566.
Adcock, I.M., Caramori, G., Kirkham, P.A., Strategies for improving the efficacy and therapeutic ratio of glucocorticoids. Curr. Opin. Pharmacol. 12 (2012), 246–251.
Caramori, G., Casolari, P., Barczyk, A., Durham, A.L., Di Stefano, A., Adcock, I., COPD immunopathology. Semin. Immunopathol. 38 (2016), 407–515.
Fabbri, N.Z., Abib-Jr, E., de Lima, Z.R., Azelastine and budesonide (nasal sprays): effect of combination therapy monitored by acoustic rhinometry and clinical symptom score in the treatment of allergic rhinitis. Allergy Rhinol. (Providence) 5 (2014), 78–86.
Rezaie, A., Kuenzig, M.E., Benchimol, E.I., Griffiths, A.M., Otley, A.R., Steinhart, A.H., Kaplan, G.G., Seow, C.H., Budesonide for induction of remission in Crohn's disease. Cochrane Database Syst. Rev., 6, 2015, CD000296.
Basu, K., Nair, A., Williamson, P.A., Mukhopadhyay, S., Lipworth, B.J., Airway and systemic effects of soluble and suspension formulations of nebulized budesonide in asthmatic children. Ann Allergy Asthma Immunol 103 (2009), 436–441.
Dufour, G., Evrard, B., de Tullio, P., Rapid quantification of 2-hydroxypropyl-beta-cyclodextrin in liquid pharmaceutical formulations by (1)H nuclear magnetic resonance spectroscopy. Eur. J. Pharm. Sci. 73 (2015), 20–28.
Kinnarinen, T., Jarho, P., Jarvinen, K., Jarvinen, T., Pulmonary deposition of a budesonide/gamma-cyclodextrin complex in vitro. J. Control. Release 90 (2003), 197–205.
Williamson, P.A., Menzies, D., Nair, A., Tutuncu, A., Lipworth, B.J., A proof-of-concept study to evaluate the antiinflammatory effects of a novel soluble cyclodextrin formulation of nebulized budesonide in patients with mild to moderate asthma. Ann Allergy Asthma Immunol 102 (2009), 161–167.
Bligh, E.G., Dyer, W.J., A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37 (1959), 911–917.
Rouser, G., Fkeischer, S., Yamamoto, A., Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 5 (1970), 494–496.
Lorent, J., Le Duff, C.S., Quetin-Leclercq, J., Mingeot-Leclercq, M.P., Induction of highly curved structures in relation to membrane permeabilization and budding by the triterpenoid saponins, alpha- and delta-Hederin. J. Biol. Chem. 288 (2013), 14000–14017.
Schroeder, F., Barenholz, Y., Gratton, E., Thompson, T.E., A fluorescence study of dehydroergosterol in phosphatidylcholine bilayer vesicles. Biochemistry 26 (1987), 2441–2448.
Cheng, K.H., Virtanen, J., Somerharju, P., Fluorescence studies of dehydroergosterol in phosphatidylethanolamine/phosphatidylcholine bilayers. Biophys. J. 77 (1999), 3108–3119.
Loura, L.M., Prieto, M., Dehydroergosterol structural organization in aqueous medium and in a model system of membranes. Biophys. J. 1997:72 (1997), 2226–2236.
Weinstein, J.N., Yoshikami, S., Henkart, P., Blumenthal, R., Hagins, W.A., Liposome-cell interaction: transfer and intracellular release of a trapped fluorescent marker. Science 195 (1977), 489–492.
Angelova, M.I., Soléau, S., Méléard, P., Faucon, J.F., Bothorel, P., Preparation of giant vesicles by external AC electric fields. Kinetics and applications. Helm, C., Lösche, M., Möhvald, H., (eds.) Trends in Colloid and Interface Science VI, 1992, Steinkopff, 127–131.
Estes, D.J., Mayer, M., Giant liposomes in physiological buffer using electroformation in a flow chamber. Biochim. Biophys. Acta 2005 (1712), 152–160.
Rodriguez, N., Pincet, F., Cribier, S., Giant vesicles formed by gentle hydration and electroformation: a comparison by fluorescence microscopy. Colloids Surf. B: Biointerfaces 42 (2005), 125–130.
Wustner, D., Fluorescent sterols as tools in membrane biophysics and cell biology. Chem. Phys. Lipids 146 (2007), 1–25.
Benesch, M.G., Lewis, R.N., McElhaney, R.N., A calorimetric and spectroscopic comparison of the effects of cholesterol and its immediate biosynthetic precursors 7-dehydrocholesterol and desmosterol on the thermotropic phase behavior and organization of dipalmitoylphosphatidylcholine bilayer membranes. Chem. Phys. Lipids 191 (2015), 123–135.
McIntosh, A.L., Gallegos, A.M., Atshaves, B.P., Storey, S.M., Kannoju, D., Schroeder, F., Fluorescence and multiphoton imaging resolve unique structural forms of sterol in membranes of living cells. J. Biol. Chem. 278 (2003), 6384–6403.
Soto-Arriaza, M.A., Olivares-Ortega, C., Quina, F.H., Aguilar, L.F., Sotomayor, C.P., Effect of cholesterol content on the structural and dynamic membrane properties of DMPC/DSPC large unilamellar bilayers. Biochim. Biophys. Acta 2013 (1828), 2763–2769.
Seras, M., Gallay, J., Vincent, M., Ollivon, M., Lesieur, S., Cholesterol assemblies induced by octyl lgucoside: a time-resolved fluorescence study of dehydroergosterol. J. Colloid Interfaces B 167 (1994), 159–171.
Ohvo-Rekila, H., Akerlund, B., Slotte, J.P., Cyclodextrin-catalyzed extraction of fluorescent sterols from monolayer membranes and small unilamellar vesicles. Chem. Phys. Lipids 105 (2000), 167–178.
Shinitzky, M., Barenholz, Y., Fluidity parameters of lipid regions determined by fluorescence polarization. Biochim. Biophys. Acta 515 (1978), 367–394.
de Almeida, R.F., Fedorov, A., Prieto, M., Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85 (2003), 2406–2416.
Puskas, I., Barcza, L., Szente, L., Csempesz, F., Features of the interaction between cyclodextrins and colloidal liposomes. J. Incl. Phenom. 54 (2006), 89–93.
Puskas, I., Csempesz, F., Influence of cyclodextrins on the physical stability of DPPC-liposomes. Colloids Surf. B: Biointerfaces 58 (2007), 218–224.
Lopez, C.A., de Vries, A.H., Marrink, S.J., Molecular mechanism of cyclodextrin mediated cholesterol extraction. PLoS Comput. Biol., 7, 2011, e1002020.
Mascetti, J., Castano, S., Cavagnat, D., Desbat, B., Organization of beta-cyclodextrin under pure cholesterol, DMPC, or DMPG and mixed cholesterol/phospholipid monolayers. Langmuir 24 (2008), 9616–9622.
Flasinski, M., Broniatowski, M., Majewski, J., Dynarowicz-Latka, P., X-ray grazing incidence diffraction and Langmuir monolayer studies of the interaction of beta-cyclodextrin with model lipid membranes. J. Colloid Interface Sci. 348 (2010), 511–521.
Lingwood, D., Simons, K., Lipid rafts as a membrane-organizing principle. Science 327 (2010), 46–50.
Irie, T., Fukunaga, K., Pitha, J., Hydroxypropylcyclodextrins in parenteral use. I: lipid dissolution and effects on lipid transfers in vitro. J. Pharm. Sci. 81 (1992), 521–523.
Ohtani, Y., Irie, T., Uekama, K., Fukunaga, K., Pitha, J., Differential effects of alpha-, beta- and gamma-cyclodextrins on human erythrocytes. Eur. J. Biochem. 186 (1989), 17–22.
Ohvo, H., Slotte, J.P., Cyclodextrin-mediated removal of sterols from monolayers: effects of sterol structure and phospholipids on desorption rate. Biochemistry 35 (1996), 8018–8024.
Christian, A.E., Haynes, M.P., Phillips, M.C., Rothblat, G.H., Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38 (1997), 2264–2272.
Rocks, N., Bekaert, S., Coia, I., Paulissen, G., Gueders, M., Evrard, B., Van Heugen, J.C., Chiap, P., Foidart, J.M., Noel, A., et al. Curcumin-cyclodextrin complexes potentiate gemcitabine effects in an orthotopic mouse model of lung cancer. Br. J. Cancer 107 (2012), 1083–1092.
Kim, J.E., Cho, H.J., Kim, D.D., Budesonide/cyclodextrin complex-loaded lyophilized microparticles for intranasal application. Drug Dev. Ind. Pharm. 40 (2014), 743–748.
Eeman, M., Francius, G., Dufrene, Y.F., Nott, K., Paquot, M., Deleu, M., Effect of cholesterol and fatty acids on the molecular interactions of fengycin with stratum corneum mimicking lipid monolayers. Langmuir 25 (2009), 3029–3039.
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