Interactions of sugar-based bolaamphiphiles with biomimetic systems of  plasma membranes

[en] Glycolipids constitute a class of molecules with various biological activities. Among them, sugar-based bolaamphiphiles characterized by their biocompatibility, biodegradability and lower toxicity, became interesting for the development of efficient and low cost lipid-based drug delivery systems. Their activity seems to be closely related to their interactions with the lipid components of the plasma membrane of target cells. Despite many works devoted to the chemical synthesis and characterization of sugar-based bolaamphiphiles, their interactions with plasma membrane have not been completely elucidated. In this work, two sugar-based bolaamphiphiles differing only at the level of their sugar residues were chemically synthetized. Their interactions with membranes have been investigated using model membranes containing or not sterol and with in silico approaches. Our findings indicate that the nature of sugar residues has no significant influence for their membrane interacting properties, while the presence of sterol attenuates the interactions of both bolaamphiphiles with the membrane systems. The understanding of this distinct behavior of bolaamphiphiles towards sterol-containing membrane systems could be useful for their applications as drug delivery systems.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Nasir, Mehmet Nail ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Chimie générale et organique

Crowet, Jean-Marc ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biophysique moléc. aux interfaces

Lins, Laurence ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biophysique moléc. aux interfaces

Obounou Akong, Firmin

Haudrechy, Arnaud

Bouquillon, Sandrine

Deleu, Magali ; Université de Liège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Biophysique moléc. aux interfaces

Language :

English

Title :

Interactions of sugar-based bolaamphiphiles with biomimetic systems of plasma membranes

Publication date :

2016

Journal title :

Biochimie

ISSN :

0300-9084

eISSN :

1638-6183

Publisher :

Elsevier, Paris, France

Volume :

130

Pages :

23-32

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www.sciencedirect.com/science/article/pii/S0300908416300438

Name of the research project :

ARC-FIELD (13/17-10), FNRS PDR NEAMEMB (T.1003.14)

Available on ORBi :

since 13 April 2016

Statistics

Number of views

121 (27 by ULiège)

Number of downloads

34 (4 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

publications

supporting

mentioning

contrasting

Smart Citations

Citing PublicationsSupportingMentioningContrasting

View Citations

See how this article has been cited at scite.ai

scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.

Bibliography

[1] Benincasa, M., Abalos, A., Oliveira, I., Manresa, A., Chemical structure, surface properties and biological activities of the biosurfactant produced by Pseudomonas aeruginosa LBI from soapstock. Antonie Van Leeuwenhoek 85 (2004), 1–8, 10.1023/B:ANTO.0000020148.45523.41.
[2] Lang, S., Wullbrandt, D., Rhamnose lipids–biosynthesis, microbial production and application potential. Appl. Microbiol. Biotechnol. 51 (1999), 22–32 http://www.ncbi.nlm.nih.gov/pubmed/10077819.
[3] Maier, R.M., Soberon-Chavez, G., Pseudomonas aeruginosa rhamnolipids: biosynthesis and potential applications. Appl. Microbiol. Biotechnol. 54 (2000), 625–633 http://www.ncbi.nlm.nih.gov/pubmed/11131386.
[4] Orgambide, G.G., Lee, J., Hollingsworth, R.I., Dazzo, F.B., Structurally diverse chitolipooligosaccharide nod factors accumulate primarily in membranes of wild type Rhizobium leguminosarum biovar trifolii. Biochemistry 34 (1995), 3832–3840 http://www.ncbi.nlm.nih.gov/pubmed/7893680.
[5] Desai, J.D., Banat, I.M., Microbial production of surfactants and their commercial potential. Microbiol. Mol. Biol. Rev. 61 (1997), 47–64 http://www.ncbi.nlm.nih.gov/pubmed/9106364.
[6] Haferburg, D., Hommel, R., Kleber, H.-P., Kluge, S., Schuster, G., Zschiegner, H.-J., Antiphytovirale Aktivität von Rhamnolipid aus Pseudomonas aeruginosa. Acta Biotechnol. 7 (1987), 353–356, 10.1002/abio.370070415.
[7] Cuvier, A.-S., Berton, J., Stevens, C.V., Fadda, G.C., Babonneau, F., Van Bogaert, I.N.A., et al. pH-triggered formation of nanoribbons from yeast-derived glycolipid biosurfactants. Soft Matter 10 (2014), 3950–3959, 10.1039/c4sm00111g.
[8] Vergne, I., Daffe, M., Interaction of mycobacterial glycolipids with host cells. Front. Biosci., 3, 1998 d865–76 http://www.ncbi.nlm.nih.gov/pubmed/9693156.
[9] Sanchez, M., Teruel, J.A., Espuny, M.J., Marques, A., Aranda, F.J., Manresa, A., et al. Modulation of the physical properties of dielaidoylphosphatidylethanolamine membranes by a dirhamnolipid biosurfactant produced by Pseudomonas aeruginosa. Chem. Phys. Lipids 142 (2006), 118–127, 10.1016/j.chemphyslip.2006.04.001.
[10] Haba, E., Pinazo, A., Pons, R., Pérez, L., Manresa, A., Complex rhamnolipid mixture characterization and its influence on DPPC bilayer organization. Biochim. Biophys. Acta 1838 (2014), 776–783, 10.1016/j.bbamem.2013.11.004.
[11] Sánchez, M., Aranda, F.J., Teruel, J.A., Ortiz, A., Interaction of a bacterial dirhamnolipid with phosphatidylcholine membranes: a biophysical study. Chem. Phys. Lipids 161 (2009), 51–55, 10.1016/j.chemphyslip.2009.06.145.
[12] Sánchez, M., Aranda, F.J., Teruel, J.A., Espuny, M.J., Marques, A., Manresa, A., et al. Permeabilization of biological and artificial membranes by a bacterial dirhamnolipid produced by Pseudomonas aeruginosa. J. Colloid Interface Sci. 341 (2010), 240–247, 10.1016/j.jcis.2009.09.042.
[13] Deleu, M., Gatard, S., Payen, E., Lins, L., Nott, K., Flore, C., et al. d-xylose-based bolaamphiphiles: synthesis and influence of the spacer nature on their interfacial and membrane properties. C. R. Chim. 15 (2012), 68–74, 10.1016/j.crci.2011.10.006.
[14] Fuhrhop, J.-H., Wang, T., Bolaamphiphiles. Chem. Rev. 104 (2004), 2901–2937, 10.1021/cr030602b.
[15] Constantinides, P.P., Tustian, A., Kessler, D.R., Tocol emulsions for drug solubilization and parenteral delivery. Adv. Drug Deliv. Rev. 56 (2004), 1243–1255, 10.1016/j.addr.2003.12.005.
[16] Jacquemet, A., Meriadec, C., Lemiegre, L., Artzner, F., Benvegnu, T., Stereochemical effect revealed in self-assemblies based on archaeal lipid analogues bearing a central five-membered carbocycle: a SAXS study. Langmuir 28 (2012), 7591–7597, 10.1021/la2045948.
[17] Jacquemet, A., Vie, V., Lemiegre, L., Barbeau, J., Benvegnu, T., Air/water interface study of cyclopentane-containing archaeal bipolar lipid analogues. Chem. Phys. Lipids 163 (2010), 794–799, 10.1016/j.chemphyslip.2010.09.005.
[18] Guilbot, J., Benvegnu, T., Legros, N., Plusquellec, D., Dedieu, J.-C., Gulik, A., Efficient synthesis of unsymmetrical bolaamphiphiles for spontaneous formation of vesicles and disks with a transmembrane organization. Langmuir 17 (2001), 613–618, 10.1021/la000892g.
[19] Kameta, N., Masuda, M., Minamikawa, H., Shimizu, T., Self-assembly and thermal phase transition behavior of unsymmetrical bolaamphiphiles having glucose- and amino-hydrophilic headgroups. Langmuir 23 (2007), 4634–4641, 10.1021/la063542o.
[20] Wu, K., Huang, M., Yue, K., Liu, C., Lin, Z., Liu, H., et al. Asymmetric giant “Bolaform-like” surfactants: precise synthesis, phase diagram, and crystallization-induced phase separation. Macromolecules 47 (2014), 4622–4633, 10.1021/ma501017e.
[21] Garelli-Calvet, R., Brisset, F., Rico, I., Lattes, A., Bis-gluconamides and bis-lactobionamides novel α,ω-type (bolaform) surfactants with two sugar head groups. Synth. Commun. 23 (1993), 35–44, 10.1080/00397919308020398.
[22] Masuda, M., Shimizu, T., Formation of complementary and cooperative hydrogen-bonding networks of sugar-based bolaamphiphiles in water. Chem. Commun., 1996, 1057, 10.1039/cc9960001057.
[23] Fuhrhop, J.H., David, H.H., Mathieu, J., Liman, U., Winter, H.J., Boekema, E., Bolaamphiphiles and monolayer lipid membranes made from 1,6,19,24-tetraoxa-3,21-cyclohexatriacontadiene-2,5,20,23-tetrone. J. Am. Chem. Soc. 108 (1986), 1785–1791, 10.1021/ja00268a013.
[24] Bertho, J.-N., Coué, A., Ewing, D.F., Goodby, J.W., Letellier, P., Mackenzie, G., et al. Novel sugar bola-amphiphiles with a pseudo macrocyclic structure. Carbohydr. Res. 300 (1997), 341–346, 10.1016/S0008-6215(97)00071-2.
[25] Clary, L., Gadras, C., Greiner, J., Rolland, J.-P., Santaella, C., Vierling, P., et al. Phase behavior of fluorocarbon and hydrocarbon double-chain hydroxylated and galactosylated amphiphiles and bolaamphiphiles. Long-term shelf-stability of their liposomes. Chem. Phys. Lipids 99 (1999), 125–137, 10.1016/S0009-3084(99)00032-8.
[26] Satge, C., Granet, R., Verneuil, B., Champavier, Y., Krausz, P., Satgé, C., Synthesis and properties of new bolaform and macrocyclic galactose-based surfactants obtained by olefin metathesis. Carbohydr. Res. 339 (2004), 1243–1254, 10.1016/j.carres.2004.03.003.
[27] Sirieix, J., Lauth–de Viguerie, N., Rivière, M., Lattes, A., From unsymmetrical bolaamphiphiles to supermolecules. New J. Chem. 24 (2000), 1043–1048, 10.1039/b005487i.
[28] Jeftić, J., Berchel, M., Mériadec, C., Benvegnu, T., Small-angle and wide-angle X-ray scattering study of slow relaxation following phase transitions of new bolaamphiphiles based on N-(12-betainylamino-dodecane)-octyl β-D-glucofuranosiduronamide chloride. Spectrosc. Lett. 45 (2012), 392–403, 10.1080/00387010.2011.611573.
[29] Gatard, S., Nasir, M.N., Deleu, M., Klai, N., Legrand, V., Bouquillon, S., Bolaamphiphiles derived from alkenyl L-rhamnosides and alkenyl D-xylosides: importance of the hydrophilic head. Molecules 18 (2013), 6101–6112, 10.3390/molecules18056101.
[30] Obounou Akong, F., Bouquillon, S., Efficient syntheses of bolaform surfactants from l -rhamnose and/or 3-(4-hydroxyphenyl)propionic acid. Green Chem. 17 (2015), 3290–3300, 10.1039/C5GC00448A.
[31] Deleu, M., Damez, C., Gatard, S., Nott, K., Paquot, M., Bouquillon, S., Synthesis and physico-chemical characterization of bolaamphiphiles derived from alkenyl d-xylosides. New J. Chem., 35, 2011, 2258, 10.1039/c1nj20158a.
[32] Marry, M., McCann, M.C., Kolpak, F., White, A.R., Stacey, N.J., Roberts, K., Extraction of pectic polysaccharides from sugar-beet cell walls. J. Sci. Food Agric. 80 (2000), 17–28, 10.1002/(SICI)1097-0010(20000101)80:1<17::AID-JSFA491>3.0.CO;2–4.
[33] Nasir, M.N., Benichou, E., Loison, C., Russier-Antoine, I., Besson, F., Brevet, P.-F.F.P.F., Influence of the tyrosine environment on the second harmonic generation of iturinic antimicrobial lipopeptides at the air-water interface. Phys. Chem. Chem. Phys. 15 (2013), 19919–19924, 10.1039/c3cp53098a.
[34] Nasir, M.N., Besson, F.F., Specific interactions of mycosubtilin with cholesterol-containing artificial membranes. Langmuir 27 (2011), 10785–10792, 10.1021/la200767e.
[35] Nsimba Zakanda, F., Lins, L., Nott, K., Paquot, M., Mvumbi Lelo, G., Deleu, M., et al. Interaction of hexadecylbetainate chloride with biological relevant lipids. Langmuir 28 (2012), 3524–3533, 10.1021/la2040328.
[36] Calvez, P., Demers, E., Boisselier, E., Salesse, C., Analysis of the contribution of saturated and polyunsaturated phospholipid monolayers to the binding of proteins. Langmuir 27 (2011), 1373–1379, 10.1021/la104097n.
[37] Calvez, P., Bussieres, S., Eric, D., Salesse, C., Bussières, S., Demers, Éric, et al. Parameters modulating the maximum insertion pressure of proteins and peptides in lipid monolayers. Biochimie 91 (2009), 718–733, 10.1016/j.biochi.2009.03.018.
[38] Nasir, M.N., Besson, F., Conformational analyses of bacillomycin D, a natural antimicrobial lipopeptide, alone or in interaction with lipid monolayers at the air–water interface. J. Colloid Interface Sci. 387 (2012), 187–193, 10.1016/j.jcis.2012.07.091.
[39] Heerklotz, H., Seelig, J., Titration calorimetry of surfactant–membrane partitioning and membrane solubilization. Biochim. Biophys. Acta – Biomembr. 1508 (2000), 69–85, 10.1016/S0304-4157(00)00009-5.
[40] Razafindralambo, H., Dufour, S., Paquot, M., Deleu, M., Thermodynamic studies of the binding interactions of surfactin analogues to lipid vesicles. J. Therm. Anal. Calorim. 95 (2009), 817–821, 10.1007/s10973-008-9403-6.
[41] Schurtenberger, P., Mazer, N., Kaenzig, W., Micelle to vesicle transition in aqueous solutions of bile salt and lecithin. J. Phys. Chem. 89 (1985), 1042–1049, 10.1021/j100252a031.
[42] Nasir, M.N., Laurent, P., Flore, C., Lins, L., Ongena, M., Deleu, M., Analysis of calcium-induced effects on the conformation of fengycin. Spectrochim. Acta. A Mol. Biomol. Spectrosc. 110 (2013), 450–457, 10.1016/j.saa.2013.03.063.
[43] Lins, L., Brasseur, R., Malaisse, W.J., Conformational analysis of non-sulfonylurea hypoglycemic agents of the meglitinide family. Biochem. Pharmacol. 50 (1995), 1879–1884 http://www.ncbi.nlm.nih.gov/pubmed/8615868.
[44] Lins, L., Thomas-Soumarmon, A., Pillot, T., Vandekerchkhove, J., Rosseneu, M., Brasseur, R., Molecular determinants of the interaction between the C-terminal domain of Alzheimer's beta-amyloid peptide and apolipoprotein E alpha-helices. J. Neurochem. 73 (1999), 758–769 http://www.ncbi.nlm.nih.gov/pubmed/10428074 (accessed 27.02.14.).
[45] Brasseur, R., Killian, J.A., De Kruijff, B., Ruysschaert, J.M., Conformational analysis of gramicidin-gramicidin interactions at the air/water interface suggests that gramicidin aggregates into tube-like structures similar as found in the gramicidin-induced hexagonal HII phase. Biochim. Biophys. Acta 903 (1987), 11–17 http://www.ncbi.nlm.nih.gov/pubmed/2443166 (accessed 27.02.14.).
[46] Nobre, T.M., Pavinatto, F.J., Caseli, L., Barros-Timmons, A., Dynarowicz-Łątka, P., Oliveira, O.N., Interactions of bioactive molecules & nanomaterials with Langmuir monolayers as cell membrane models. Thin Solid Films 593 (2015), 158–188, 10.1016/j.tsf.2015.09.047.
[47] Deleu, M., Crowet, J.-M., Nasir, M.N., Lins, L., Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: a review. Biochim. Biophys. Acta 1838 (2014), 3171–3190, 10.1016/j.bbamem.2014.08.023.
[48] Maget-Dana, R., Ptak, M., Interactions of surfactin with membrane models. Biophys. J. 68 (1995), 1937–1943, 10.1016/S0006-3495(95)80370-X.
[49] Marsh, D., Lateral pressure in membranes. Biochim. Biophys. Acta 1286 (1996), 183–223 http://www.ncbi.nlm.nih.gov/pubmed/8982283 (accessed 21.02.14.).
[50] Zhao, H., Sood, R., Jutila, A., Bose, S., Fimland, G., Nissen-Meyer, J., et al. Interaction of the antimicrobial peptide pheromone Plantaricin A with model membranes: implications for a novel mechanism of action. Biochim. Biophys. Acta 1758 (2006), 1461–1474, 10.1016/j.bbamem.2006.03.037.
[51] Miñones, J., Pais, S., Conde, O., Dynarowicz-Łatka, P., Interactions between membrane sterols and phospholipids in model mammalian and fungi cellular membranes–a Langmuir monolayer study. Biophys. Chem. 140 (2009), 69–77, 10.1016/j.bpc.2008.11.011.
[52] Mitchell, D.C., Litman, B.J., Effect of cholesterol on molecular order and dynamics in highly polyunsaturated phospholipid bilayers. Biophys. J. 75 (1998), 896–908, 10.1016/S0006-3495(98)77578-2.
[53] J. Hernández, A. Martí, J. Estelrich, Interaction of doxorubicin with lipid systems, Bioconjug. Chem. 2 398–402. http://www.ncbi.nlm.nih.gov/pubmed/1805935 (accessed 16.03.16.).
[54] Ibdah, J.A., Phillips, M.C., Effects of lipid composition and packing on the adsorption of apolipoprotein A-I to lipid monolayers. Biochemistry 27 (1988), 7155–7162 http://www.ncbi.nlm.nih.gov/pubmed/3143410 (accessed 16.03.16.).
[55] Bouchemal, K., New challenges for pharmaceutical formulations and drug delivery systems characterization using isothermal titration calorimetry. Drug Discov. Today 13 (2008), 960–972, 10.1016/j.drudis.2008.06.004.
[56] Prenner, E.J., Lewis, R.N.A.H., Jelokhani-Niaraki, M., Hodges, R.S., McElhaney, R.N., Cholesterol attenuates the interaction of the antimicrobial peptide gramicidin S with phospholipid bilayer membranes. Biochim. Biophys. Acta – Biomembr. 1510 (2001), 83–92, 10.1016/S0005-2736(00)00337-0.
[57] Verly, R.M., Rodrigues, M.A., Daghastanli, K.R.P., Denadai, A.M.L., Cuccovia, I.M., Bloch, C., et al. Effect of cholesterol on the interaction of the amphibian antimicrobial peptide DD K with liposomes. Peptides 29 (2008), 15–24, 10.1016/j.peptides.2007.10.028.
[58] Ter-Minassian-Saraga, L., Okamura, E., Umemura, J., Takenaka, T., Fourier transform infrared-attenuated total reflection spectroscopy of hydration of dimyristoylphosphatidylcholine multibilayers. Biochim. Biophys. Acta – Biomembr. 946 (1988), 417–423, 10.1016/0005-2736(88)90417-8.
[59] Blume, A., Hübner, W., Messner, G., Fourier transform infrared spectroscopy of 13C=O-labeled phospholipids hydrogen bonding to carbonyl groups. Biochemistry 27 (1988), 8239–8249 http://www.scopus.com/inward/record.url?eid=2-s2.0-0024291319&partnerID=tZOtx3y1.
[60] Jiao, T., Gao, F., Zhang, Q., Zhou, J., Gao, F., Spacer effect on nanostructures and self-assembly in organogels via some bolaform cholesteryl imide derivatives with different spacers. Nanoscale Res. Lett., 8, 2013, 406, 10.1186/1556-276X-8-406.
[61] Forbes, C.C., DiVittorio, K.M., Smith, B.D., Bolaamphiphiles promote phospholipid translocation across vesicle membranes. J. Am. Chem. Soc. 128 (2006), 9211–9218, 10.1021/ja0619253.
[62] Meister, A., K?hler, K., Drescher, S., Dobner, B., Karlsson, G., Edwards, K., et al. Mixing behaviour of a symmetrical single-chain bolaamphiphile with phospholipids. Soft Matter, 3, 2007, 1025, 10.1039/b703152a.
[63] Fraile, M.V., Patrón-Gallardo, B., López-Rodrı́guez, G., Carmona, P., FT-IR study of multilamellar lipid dispersions containing cholesteryl linoleate and dipalmitoylphosphatidylcholine. Chem. Phys. Lipids 97 (1999), 119–128, 10.1016/S0009-3084(98)00103-0.
[64] Bottier, C., Géan, J., Artzner, F., Desbat, B., Pézolet, M., Renault, A., et al. Galactosyl headgroup interactions control the molecular packing of wheat lipids in Langmuir films and in hydrated liquid-crystalline mesophases. Biochim. Biophys. Acta 1768 (2007), 1526–1540, 10.1016/j.bbamem.2007.02.021.
[65] McMullen, T.P., McElhaney, R.N., Physical studies of cholesterol-phospholipid interactions. Curr. Opin. Colloid Interface Sci. 1 (1996), 83–90, 10.1016/S1359-0294(96)80048-3.
[66] Lohner, K., Prenner, E.J., Differential scanning calorimetry and X-ray diffraction studies of the specificity of the interaction of antimicrobial peptides with membrane-mimetic systems. Biochim. Biophys. Acta – Biomembr. 1462 (1999), 141–156, 10.1016/S0005-2736(99)00204-7.
[67] Owen, J.S., Bruckdorfer, K.R., Day, R.C., McIntyre, N., Decreased erythrocyte membrane fluidity and altered lipid composition in human liver disease. J. Lipid Res. 23 (1982), 124–132 http://www.ncbi.nlm.nih.gov/pubmed/7057101 (accessed 11.12.15.).
[68] Sahu, S., Lynn, W.S., Lipid composition of human alveolar macrophages. Inflammation 2 (1977), 83–91, 10.1007/BF00918670.

Similar publications

Sorry the service is unavailable at the moment. Please try again later.

Name	Provider / Domaine	Expiration	Description
JSESSIONID	Oracle Corporation www.uliege.be	Session	General purpose platform session cookie, used by sites written in JSP. Usually used to maintain an anonymous user session by the server.
CookieScriptConsent	CookieScript .uliege.be	1 year	This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.

Name	Provider / Domaine	Expiration	Description
_pk_id	InnoCraft Ltd .uliege.be	1 year	Used to store a few details about the user such as the unique visitor ID
_pk_ses	InnoCraft Ltd .uliege.be	30 minutes	Short lived cookies used to temporarily store data for the visit
_pk_ref	InnoCraft Ltd .uliege.be	6 months	Used to store the attribution information, the referrer initially used to visit the website