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Drug Delivery Letters

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ISSN (Print): 2210-3031
ISSN (Online): 2210-304X

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Letter Article

Plasma Protein Adsorption on Melphalan Prodrug Bearing Liposomes - Bare, Stealth, and Targeted

Author(s): Maria Kobanenko, Pavel Samofalov, Irina Kapitonova, Anna Alekseeva, Marina Kapkaeva, Olga Scheglovitova, Alexander Tuzikov, Daria Tretiakova* and Elena Vodovozova

Volume 14, Issue 4, 2024

Published on: 27 June, 2024

Page: [320 - 328] Pages: 9

DOI: 10.2174/0122103031297263240612110749

Price: $65

Abstract

Background: Plasma protein binding is inevitable for nanomaterials injected into blood circulation. For liposomes, this process is affected by the lipid composition of the bilayer. Membrane constituents and their ratio define liposome characteristics, namely, surface charge and hydrophobicity, which drive protein adsorption. Roughly 30 years ago, the correlation between the amount of bound proteins and the resulting circulation time of liposomes was established by S. Semple, A. Chonn, and P. Cullis. Here, we have estimated ex vivo plasma protein binding, primarily to determine the impact of melphalan prodrug inclusion into bilayer on bare, PEGylated (stealth), and Sialyl Lewis X (SiaLeX)-decorated liposomes.

Experimental: Liposomes were allowed to bind plasma proteins for 15 minutes, then liposome-protein complexes were isolated, and protein and lipid quantities were assessed in the complexes. In addition, the uptake by activated HUVEC cells was evaluated for SiaLeX-decorated liposomes.

Results: Melphalan moieties on the bilayer surface enrich protein adsorption compared to pure phosphatidylcholine sample. Although PEG-lipid had facilitated a significant decrease in protein adsorption in the control sample, when prodrug was added to the composition, the degree of protein binding was restored to the level of melphalan liposomes without a stealth barrier. A similar effect was observed for SiaLeX-decorated liposomes.

Conclusion: None of the compositions reported here should suffer from quick elimination from circulation, according to the cut-off values introduced by Cullis and colleagues. Nevertheless, the amount of bound proteins is sufficient to affect biodistribution, namely, to impair receptor recognition of SiaLeX and reduce liposome uptake by endothelial cells.

« Previous Next »
[1]
Bulbake, U.; Doppalapudi, S.; Kommineni, N.; Khan, W. Liposomal formulations in clinical use: An updated review. Pharmaceutics, 2017, 9(4), 12.
[http://dx.doi.org/10.3390/pharmaceutics9020012] [PMID: 28346375]
[2]
Large, D.E.; Abdelmessih, R.G.; Fink, E.A.; Auguste, D.T. Liposome composition in drug delivery design, synthesis, characterization, and clinical application. Adv. Drug Deliv. Rev., 2021, 176, 113851.
[http://dx.doi.org/10.1016/j.addr.2021.113851] [PMID: 34224787]
[3]
Nsairat, H.; Khater, D.; Sayed, U.; Odeh, F.; Al Bawab, A.; Alshaer, W. Liposomes: Structure, composition, types, and clinical applications. Heliyon, 2022, 8(5), e09394.
[http://dx.doi.org/10.1016/j.heliyon.2022.e09394] [PMID: 35600452]
[4]
Tseu, G.Y.W.; Kamaruzaman, K.A. A review of different types of liposomes and their advancements as a form of gene therapy treatment for breast cancer. Molecules, 2023, 28(3), 1498.
[http://dx.doi.org/10.3390/molecules28031498] [PMID: 36771161]
[5]
Zylberberg, C.; Matosevic, S. Pharmaceutical liposomal drug delivery: A review of new delivery systems and a look at the regulatory landscape. Drug Deliv., 2016, 23(9), 3319-3329.
[http://dx.doi.org/10.1080/10717544.2016.1177136] [PMID: 27145899]
[6]
Fulton, M.D.; Najahi-Missaoui, W. Liposomes in cancer therapy: How did we start and where are we now. Int. J. Mol. Sci., 2023, 24(7), 6615.
[http://dx.doi.org/10.3390/ijms24076615] [PMID: 37047585]
[7]
Onishchenko, N.; Tretiakova, D.; Vodovozova, E. Spotlight on the protein corona of liposomes. Acta Biomater., 2021, 134, 57-78.
[http://dx.doi.org/10.1016/j.actbio.2021.07.074] [PMID: 34364016]
[8]
Quagliarini, E.; Digiacomo, L.; Renzi, S.; Pozzi, D.; Caracciolo, G. A decade of the liposome-protein corona: Lessons learned and future breakthroughs in theranostics. Nano Today, 2022, 47, 101657.
[http://dx.doi.org/10.1016/j.nantod.2022.101657]
[9]
Singh, N.; Marets, C.; Boudon, J.; Millot, N.; Saviot, L.; Maurizi, L. In vivo protein corona on nanoparticles: Does the control of all material parameters orient the biological behavior? Nanoscale Adv., 2021, 3(5), 1209-1229.
[http://dx.doi.org/10.1039/D0NA00863J] [PMID: 36132858]
[10]
Lasic, D.D.; Martin, F.J.; Gabizon, A.; Huang, S.K.; Papahadjopoulos, D. Sterically stabilized liposomes: A hypothesis on the molecular origin of the extended circulation times. Biochim. Biophys. Acta Biomembr., 1991, 1070(1), 187-192.
[http://dx.doi.org/10.1016/0005-2736(91)90162-2] [PMID: 1751525]
[11]
Allen, T.M.; Hansen, C.; Rutledge, J. Liposomes with prolonged circulation times: Factors affecting uptake by reticuloendothelial and other tissues. Biochim. Biophys. Acta Biomembr., 1989, 981(1), 27-35.
[http://dx.doi.org/10.1016/0005-2736(89)90078-3] [PMID: 2719971]
[12]
Storm, G.; Belliot, S.O.; Daemen, T.; Lasic, D.D. Surface modification of nanoparticles to oppose uptake by the mononuclear phagocyte system. Adv. Drug Deliv. Rev., 1995, 17(1), 31-48.
[http://dx.doi.org/10.1016/0169-409X(95)00039-A]
[13]
Liu, T.; Choi, H.; Zhou, R.; Chen, I.W. RES blockade: A strategy for boosting efficiency of nanoparticle drug. Nano Today, 2015, 10(1), 11-21.
[http://dx.doi.org/10.1016/j.nantod.2014.12.003]
[14]
Chonn, A.; Semple, S.C.; Cullis, P.R. Association of blood proteins with large unilamellar liposomes in vivo relation to circulation lifetimes. J. Biol. Chem., 1992, 267(26), 18759-18765.
[http://dx.doi.org/10.1016/S0021-9258(19)37026-7] [PMID: 1527006]
[15]
Semple, S.C.; Chonn, A.; Cullis, P.R. Interactions of liposomes and lipid-based carrier systems with blood proteins: Relation to clearance behaviour in vivo. Adv. Drug Deliv. Rev., 1998, 32(1-2), 3-17.
[http://dx.doi.org/10.1016/S0169-409X(97)00128-2] [PMID: 10837632]
[16]
Di, J.; Gao, X.; Du, Y.; Zhang, H.; Gao, J.; Zheng, A. Size, shape, charge and “stealthy” surface: Carrier properties affect the drug circulation time in vivo. Asian J. Pharm. Sci., 2021, 16(4), 444-458.
[http://dx.doi.org/10.1016/j.ajps.2020.07.005] [PMID: 34703494]
[17]
Ibrahim, M.; Ramadan, E.; Elsadek, N.E.; Emam, S.E.; Shimizu, T.; Ando, H.; Ishima, Y.; Elgarhy, O.H.; Sarhan, H.A.; Hussein, A.K.; Ishida, T. Polyethylene glycol (PEG): The nature, immunogenicity, and role in the hypersensitivity of PEGylated products. J. Control. Release, 2022, 351, 215-230.
[http://dx.doi.org/10.1016/j.jconrel.2022.09.031] [PMID: 36165835]
[18]
Zalba, S.; ten Hagen, T.L.M.; Burgui, C.; Garrido, M.J. Stealth nanoparticles in oncology: Facing the PEG dilemma. J. Control. Release, 2022, 351, 22-36.
[http://dx.doi.org/10.1016/j.jconrel.2022.09.002] [PMID: 36087801]
[19]
Münter, R.; Stavnsbjerg, C.; Christensen, E.; Thomsen, M.E.; Stensballe, A.; Hansen, A.E.; Parhamifar, L.; Kristensen, K.; Simonsen, J.B.; Larsen, J.B.; Andresen, T.L. Unravelling heterogeneities in complement and antibody opsonization of individual liposomes as a function of surface architecture. Small, 2022, 18(14), 2106529.
[http://dx.doi.org/10.1002/smll.202106529] [PMID: 35187804]
[20]
Schöttler, S.; Becker, G.; Winzen, S.; Steinbach, T.; Mohr, K.; Landfester, K.; Mailänder, V.; Wurm, F.R. Protein adsorption is required for stealth effect of poly(ethylene glycol)- and poly(phosphoester)-coated nanocarriers. Nat. Nanotechnol., 2016, 11(4), 372-377.
[http://dx.doi.org/10.1038/nnano.2015.330] [PMID: 26878141]
[21]
Rampado, R.; Crotti, S.; Caliceti, P.; Pucciarelli, S.; Agostini, M. Recent advances in understanding the protein corona of nanoparticles and in the formulation of “stealthy” nanomaterials. Front. Bioeng. Biotechnol., 2020, 8, 166.
[http://dx.doi.org/10.3389/fbioe.2020.00166] [PMID: 32309278]
[22]
Xiao, Q.; Zoulikha, M.; Qiu, M.; Teng, C.; Lin, C.; Li, X.; Sallam, M.A.; Xu, Q.; He, W. The effects of protein corona on in vivo fate of nanocarriers. Adv. Drug Deliv. Rev., 2022, 186, 114356.
[http://dx.doi.org/10.1016/j.addr.2022.114356] [PMID: 35595022]
[23]
Zhang, Z.; Guan, J.; Jiang, Z.; Yang, Y.; Liu, J.; Hua, W.; Mao, Y.; Li, C.; Lu, W.; Qian, J.; Zhan, C. Brain-targeted drug delivery by manipulating protein corona functions. Nat. Commun., 2019, 10(1), 3561.
[http://dx.doi.org/10.1038/s41467-019-11593-z] [PMID: 31395892]
[24]
Li, H.; Yin, D.; Liao, J.; Wang, Y.; Gou, R.; Tang, C.; Li, W.; Liu, Y.; Fu, J.; Shi, S.; Zou, L. Regulation of protein corona on liposomes using albumin-binding peptide for targeted tumor therapy. J. Control. Release, 2023, 355, 593-603.
[http://dx.doi.org/10.1016/j.jconrel.2023.02.004] [PMID: 36773961]
[25]
Foxall, C.; Watson, S.R.; Dowbenko, D.; Fennie, C.; Lasky, L.A.; Kiso, M.; Hasegawa, A.; Asa, D.; Brandley, B.K. The three members of the selectin receptor family recognize a common carbohydrate epitope, the sialyl Lewis(x) oligosaccharide. J. Cell Biol., 1992, 117(4), 895-902.
[http://dx.doi.org/10.1083/jcb.117.4.895] [PMID: 1374413]
[26]
Ganesh, D.; Jain, P.; Shanthamurthy, C.D.; Toraskar, S.; Kikkeri, R. Targeting selectins mediated biological activities with multivalent probes. Front Chem., 2021, 9, 773027.
[http://dx.doi.org/10.3389/fchem.2021.773027] [PMID: 34926401]
[27]
Kuznetsova, N.R.; Stepanova, E.V.; Peretolchina, N.M.; Khochenkov, D.A.; Boldyrev, I.A.; Bovin, N.V.; Vodovozova, E.L. Targeting liposomes loaded with melphalan prodrug to tumour vasculature via the Sialyl Lewis X selectin ligand. J. Drug Target., 2014, 22(3), 242-250.
[http://dx.doi.org/10.3109/1061186X.2013.862805] [PMID: 24313904]
[28]
Semple, S.C.; Chonn, A. Liposome-blood protein interactions in relation to liposome clearance. J. Liposome Res., 1996, 6(1), 33-60.
[http://dx.doi.org/10.3109/08982109609037201]
[29]
Dos Santos, N.; Allen, C.; Doppen, A.M.; Anantha, M.; Cox, K.A.K.; Gallagher, R.C.; Karlsson, G.; Edwards, K.; Kenner, G.; Samuels, L.; Webb, M.S.; Bally, M.B. Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: Relating plasma circulation lifetimes to protein binding. Biochim. Biophys. Acta Biomembr., 2007, 1768(6), 1367-1377.
[http://dx.doi.org/10.1016/j.bbamem.2006.12.013] [PMID: 17400180]
[30]
Tretiakova, D.; Svirshchevskaya, E.; Onishchenko, N.; Alekseeva, A.; Boldyrev, I.; Kamyshinsky, R.; Natykan, A.; Lokhmotov, A.; Arantseva, D.; Shobolov, D.; Vodovozova, E. Liposomal formulation of a melphalan lipophilic prodrug: Studies of acute toxicity, tolerability, and antitumor efficacy. Curr. Drug Deliv., 2020, 17(4), 312-323.
[http://dx.doi.org/10.2174/1567201817666200214105357] [PMID: 32056524]
[31]
Tuzikov, A.B.; Ryabukhina, E.V.; Paramonov, A.S.; Chizhov, A.O.; Bovin, N.V.; Vodovozova, E.L. A convenient route to conjugates of 1,2-diglycerides with functionalized oligoethylene glycol spacer arms. Mendeleev Commun., 2021, 31(4), 538-541.
[http://dx.doi.org/10.1016/j.mencom.2021.07.034]
[32]
Boldyrev, I.A.; Zhai, X.; Momsen, M.M.; Brockman, H.L.; Brown, R.E.; Molotkovsky, J.G. New BODIPY lipid probes for fluorescence studies of membranes. J. Lipid Res., 2007, 48(7), 1518-1532.
[http://dx.doi.org/10.1194/jlr.M600459-JLR200] [PMID: 17416929]
[33]
Onishchenko, N.R.; Moskovtsev, A.A.; Kobanenko, M.K.; Tretiakova, D.S.; Alekseeva, A.S.; Kolesov, D.V.; Mikryukova, A.A.; Boldyrev, I.A.; Kapkaeva, M.R.; Shcheglovitova, O.N.; Bovin, N.V.; Kubatiev, A.A.; Tikhonova, O.V.; Vodovozova, E.L. Protein corona attenuates the targeting of antitumor sialyl lewis X-decorated liposomes to vascular endothelial cells under flow conditions. Pharmaceutics, 2023, 15(6), 1754.
[http://dx.doi.org/10.3390/pharmaceutics15061754] [PMID: 37376203]
[34]
Tretiakova, D.; Kobanenko, M.; Alekseeva, A.; Boldyrev, I.; Khaidukov, S.; Zgoda, V.; Tikhonova, O.; Vodovozova, E.; Onishchenko, N. Protein corona of anionic fluid-phase liposomes compromises their integrity rather than uptake by cells. Membranes, 2023, 13(7), 681.
[http://dx.doi.org/10.3390/membranes13070681] [PMID: 37505047]
[35]
Münter, R.; Simonsen, J.B. Comment on “Optimal centrifugal isolating of liposome-protein complexes from human plasma” by L. Digiacomo, F. Giulimondi, A. L. Capriotti, S. Piovesana, C. M. Montone, R. Z. Chiozzi, A. Laganá, M. Mahmoudi, D. Pozzi and G. Caracciolo, Nanoscale Adv., 2021, 3, 3824. Nanoscale Adv., 2022, 5(1), 290-299.
[http://dx.doi.org/10.1039/D2NA00343K] [PMID: 36605796]
[36]
Markwell, M.A.K.; Haas, S.M.; Bieber, L.L.; Tolbert, N.E. A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal. Biochem., 1978, 87(1), 206-210.
[http://dx.doi.org/10.1016/0003-2697(78)90586-9] [PMID: 98070]
[37]
Tretiakova, D.; Kobanenko, M.; Le-Deygen, I.; Boldyrev, I.; Kudryashova, E.; Onishchenko, N.; Vodovozova, E. Spectroscopy study of albumin interaction with negatively charged liposome membranes: Mutual structural effects of the protein and the bilayers. Membranes, 2022, 12(11), 1031.
[http://dx.doi.org/10.3390/membranes12111031] [PMID: 36363586]
[38]
Jaffe, E.A.; Nachman, R.L.; Becker, C.G.; Minick, C.R. Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J. Clin. Invest., 1973, 52(11), 2745-2756.
[http://dx.doi.org/10.1172/JCI107470] [PMID: 4355998]
[39]
Scheglovitova, O.N.; Romanov, Y.A.; Maksianina, E.V.; Svintsitskaya, V.A.; Pronin, A.G. Herpes simplex type I virus infected human vascular endothelial cells induce the production of anti-viral and proinflammatory factors by peripheral blood leukocytes in vitro. Russ. J. Immunol., 2002, 7(2), 115-122.
[PMID: 12687253]
[40]
Delacre, M.; Leys, C.; Mora, Y.L.; Lakens, D. Taking parametric assumptions seriously: Arguments for the use of Welch’s F-test instead of the classical F-test in one-way ANOVA. Rev. Int. Psychol. Soc., 2019, 32(1), 13.
[http://dx.doi.org/10.5334/irsp.198]
[41]
Barba-Bon, A.; Nilam, M.; Hennig, A. Supramolecular chemistry in the biomembrane. ChemBioChem, 2020, 21(7), 886-910.
[http://dx.doi.org/10.1002/cbic.201900646] [PMID: 31803982]
[42]
Le Grandois, J.; Marchioni, E.; Zhao, M.; Giuffrida, F.; Ennahar, S.; Bindler, F. Investigation of natural phosphatidylcholine sources: Separation and identification by liquid chromatography-electrospray ionization-tandem mass spectrometry (LC-ESI-MS2) of molecular species. J. Agric. Food Chem., 2009, 57(14), 6014-6020.
[http://dx.doi.org/10.1021/jf900903e] [PMID: 19545117]
[43]
Tretiakova, D.; Onishchenko, N.; Boldyrev, I.; Mikhalyov, I.; Tuzikov, A.; Bovin, N.; Evtushenko, E.; Vodovozova, E. Influence of stabilizing components on the integrity of antitumor liposomes loaded with lipophilic prodrug in the bilayer. Colloids Surf. B Biointerfaces, 2018, 166, 45-53.
[http://dx.doi.org/10.1016/j.colsurfb.2018.02.061] [PMID: 29533843]
[44]
Silvius, J.R.; Zuckermann, M.J. Interbilayer transfer of phospholipid-anchored macromolecules via monomer diffusion. Biochemistry, 1993, 32(12), 3153-3161.
[http://dx.doi.org/10.1021/bi00063a030] [PMID: 7681327]
[45]
Berger, M.; Degey, M.; Leblond Chain, J.; Maquoi, E.; Evrard, B.; Lechanteur, A.; Piel, G. Effect of PEG anchor and serum on lipid nanoparticles: Development of a nanoparticles tracking method. Pharmaceutics, 2023, 15(2), 597.
[http://dx.doi.org/10.3390/pharmaceutics15020597] [PMID: 36839919]
[46]
Kristensen, K.; Urquhart, A.J.; Thormann, E.; Andresen, T.L. Binding of human serum albumin to PEGylated liposomes: Insights into binding numbers and dynamics by fluorescence correlation spectroscopy. Nanoscale, 2016, 8(47), 19726-19736.
[http://dx.doi.org/10.1039/C6NR05455B] [PMID: 27874129]
[47]
Tretiakova, D.; Le-Deigen, I.; Onishchenko, N.; Kuntsche, J.; Kudryashova, E.; Vodovozova, E. Phosphatidylinositol Stabilizes Fluid-Phase Liposomes Loaded with a Melphalan Lipophilic Prodrug. Pharmaceutics, 2021, 13(4), 473.
[http://dx.doi.org/10.3390/pharmaceutics13040473] [PMID: 33915726]
[48]
Salvati, A.; Pitek, A.S.; Monopoli, M.P.; Prapainop, K.; Bombelli, F.B.; Hristov, D.R.; Kelly, P.M.; Åberg, C.; Mahon, E.; Dawson, K.A. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol., 2013, 8(2), 137-143.
[http://dx.doi.org/10.1038/nnano.2012.237] [PMID: 23334168]
[49]
Francia, V.; Yang, K.; Deville, S.; Reker-Smit, C.; Nelissen, I.; Salvati, A. Corona composition can affect the mechanisms cells use to internalize nanoparticles. ACS Nano, 2019, 13(10), 11107-11121.
[http://dx.doi.org/10.1021/acsnano.9b03824] [PMID: 31525954]
[50]
Yang, K.; Reker-Smit, C.; Stuart, M.C.A.; Salvati, A. Effects of protein source on liposome uptake by cells: Corona composition and impact of the excess free proteins. Adv. Healthc. Mater., 2021, 10(14), 2100370.
[http://dx.doi.org/10.1002/adhm.202100370] [PMID: 34050634]
[51]
Murray, K.S.; Rouse, J.C.; Tangarone, B.S.; Peterson, K.A.; Van Cleave, V.H. Identification of human serum interferants in the recombinant P-selectin glycoprotein ligand-1 clinical ELISA using MALDI MS and RP-HPLC. J. Immunol. Methods, 2001, 255(1-2), 41-56.
[http://dx.doi.org/10.1016/S0022-1759(01)00421-5] [PMID: 11470285]
[52]
Marques, C.; Hajipour, M.J.; Marets, C.; Oudot, A.; Safavi-sohi, R.; Guillemin, M.; Borchard, G.; Jordan, O.; Saviot, L.; Maurizi, L. Identification of the proteins determining the blood circulation time of nanoparticles. ACS Nano, 2023, 17(13), 12458-12470.
[http://dx.doi.org/10.1021/acsnano.3c02041] [PMID: 37379064]

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