Cubosomes: The Next Generation of Smart Lipid Nanoparticles?
Dr. Hanna M. G. Barriga
Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
Search for more papers by this authorDr. Margaret N. Holme
Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
Search for more papers by this authorCorresponding Author
Prof. Molly M. Stevens
Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
Departments of Materials and Bioengineering and Institute of Biomedical Engineering, Imperial College London, London, UK
Search for more papers by this authorDr. Hanna M. G. Barriga
Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
Search for more papers by this authorDr. Margaret N. Holme
Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
Search for more papers by this authorCorresponding Author
Prof. Molly M. Stevens
Department of Medical Biochemistry and Biophysics, Karolinska Institute, Stockholm, Sweden
Departments of Materials and Bioengineering and Institute of Biomedical Engineering, Imperial College London, London, UK
Search for more papers by this authorGraphical Abstract
Cubosomes are nanoparticles with an internal periodic lipid membrane separated by two distinct water channels. The surface is stabilized by a polymer outer corona. Recent advances have enabled the rational design of cubosome systems. Key considerations are outlined for engineering cubosomes for tailor-made applications including delivery, biosensing, and medical applications.
Abstract
Cubosomes are highly stable nanoparticles formed from the lipid cubic phase and stabilized by a polymer based outer corona. Bicontinuous lipid cubic phases consist of a single lipid bilayer that forms a continuous periodic membrane lattice structure with pores formed by two interwoven water channels. Cubosome composition can be tuned to engineer pore sizes or include bioactive lipids, the polymer outer corona can be used for targeting and they are highly stable under physiological conditions. Compared to liposomes, the structure provides a significantly higher membrane surface area for loading of membrane proteins and small drug molecules. Owing to recent advances, they can be engineered in vitro in both bulk and nanoparticle formats with applications including drug delivery, membrane bioreactors, artificial cells, and biosensors. This review outlines recent advances in cubosome technology enabling their application and provides guidelines for the rational design of new systems for biomedical applications.
Conflict of interest
The authors declare no conflict of interest.
References
- 1G. van Meer, D. R. Voelker, G. W. Feigenson, Nat. Rev. Mol. Cell Biol. 2008, 9, 112–24.
- 2N. Stepanyants, P. J. Macdonald, C. A. Francy, J. A. Mears, X. Qi, R. Ramachandrana, Mol. Biol. Cell 2015, 26, 3104–3116.
- 3M. Simunovic, E. Evergren, I. Golushko, C. Prévost, H.-F. Renard, L. Johannes, H. T. McMahon, V. Lorman, G. A. Voth, P. Bassereau, Proc. Natl. Acad. Sci. USA 2016, 113, 11226–11231.
- 4A. Schmidt, M. Wolde, C. Thiele, W. Fest, H. Kratzin, A. V. Podtelejnikov, W. Witke, W. B. Huttner, H.-D. Söling, Nature 1999, 401, 133–141.
- 5Y. Deng, M. Marko, K. F. Buttle, A. Leith, M. Mieczkowski, C. A. Mannella, J. Struct. Biol. 1999, 127, 231–239.
- 6B. D. Wilts, B. Apeleo Zubiri, M. A. Klatt, B. Butz, M. G. Fischer, S. T. Kelly, E. Spiecker, U. Steiner, G. E. Schröder-Turk, Sci. Adv. 2017, 3, e 1603119.
- 7G. E. Schröder-Turk, S. Wickham, H. Averdunk, F. Brink, J. D. Fitz Gerald, L. Poladian, M. C. Large, S. T. Hyde, J. Struct. Biol. 2011, 174, 290–295.
- 8A. Jesorka, O. Orwar, Annu. Rev. Anal. Chem. 2008, 1, 801–832.
- 9J. Gustafsson, H. Ljusberg-Wahren, M. Almgren, K. Larsson, Langmuir 1996, 12, 4611–4613.
- 10M. Lindström, H. Ljusberg-Wahren, K. Larsson, B. Borgström, Lipids 1981, 16, 749–754.
- 11G. van Meer, A. I. P. M. de Kroon, J. Cell Sci. 2011, 124, 5–8.
- 12M. P. Wymann, R. Schneiter, Nat. Rev. Mol. Cell Biol. 2008, 9, 162–176.
- 13M. Hilyo, C. Denkert, L. Lehtinen, B. Müller, S. Brockmöller, T. Seppänen-Laakso, J. Budczies, E. Bucher, L. Yetukuri, S. Castillo, et al., Cancer Res. 2011, 71, 3236–3245.
- 14S. Beloribi-Djefaflia, S. Vasseur, F. Guillaumond, Oncogenesis 2016, 5, e 189.
- 15L. Puglielli, R. E. Tanzi, D. M. Kovacs, Nat. Neurosci. 2003, 6, 345–351.
- 16S. Askarova, X. Yang, J. C. Lee, Int. J. Alzheimers Dis. 2011, 134971.
- 17A. Walter, U. Korth, M. Hilgert, J. Hartmann, O. Weichel, M. Hilgert, K. Fassbender, A. Schmitt, J. Klein, Neurobiol. Aging 2004, 25, 1299–1303.
- 18F. R. Maxfield, I. Tabas, Nature 2005, 438, 612–621.
- 19S. Spiegel, S. Milstien, Nat. Rev. Mol. Cell Biol. 2003, 4, 397–407.
- 20J. M. Seddon, R. H. Templer, Chapter 3, Polymorphism of Lipid–Water Systems, Handbook of Biological Physics, Elsevier Science B. V., North Holland, 1995.
- 21G. C. Shearman, O. Ces, R. H. Templer, J. M. Seddon, J. Phys. Condens. Matter 2006, 18, S 1105–S1124.
- 22O. Ces, X. Mulet, Signal Transduct. 2006, 6, 112–132.
- 23A. Yaghmur, O. Glatter, Adv. Colloid Interface Sci. 2009, 147–148, 333–342.
- 24P. T. Spicer, Curr. Opin. Colloid Interface Sci. 2005, 10, 274–279.
- 25I. Azmi, S. Moghimi, A. Yaghmur, Ther. Delivery 2015, 6, 1347–1364.
- 26A. Chemelli, M. Maurer, R. Geier, O. Glatter, Langmuir 2012, 28, 16788–16797.
- 27J. Barauskas, M. Johnsson, F. Tiberg, Nano Lett. 2005, 5, 1615–1619.
- 28C. V. Kulkarni, W. Wachter, G. Iglesias-Salto, S. Engelskirchen, S. Ahualli, Phys. Chem. Chem. Phys. 2011, 13, 3004–3021.
- 29M. Caffrey, Biochemistry 1987, 26, 6349–6363.
- 30J. Barauskas, T. Landh, Langmuir 2003, 19, 9562–9565.
- 31T. Landh, J. Phys. Chem. B 1994, 98, 8453–8467.
- 32C. Caltagirone, A. M. Falchi, S. Lampis, V. Lippolis, V. Meli, M. Monduzzi, L. Prodi, J. Schmidt, M. Sgarzi, Y. Talmon, et al., Langmuir 2014, 30, 6228–6236.
- 33D. Demurtas, P. Guichard, I. Martiel, R. Mezzenga, C. Herbert, L. Sagalowicz, Nat. Commun. 2015, 6, 8915.
- 34M. Duss, L. S. Manni, L. Moser, S. Handschin, R. Mezzenga, H. J. Jessen, E. M. Landau, ACS Appl. Mater. Interfaces 2018, 10, 5114–5124.
- 35S. Deshpande, E. Venugopal, S. Ramagiri, J. R. Bellare, G. Kumaraswamy, N. Singh, ACS Appl. Mater. Interfaces 2014, 6, 17126–17133.
- 36J. Gustafsson, H. Ljusberg-wahren, M. Almgren, Langmuir 1997, 13, 6964–6971.
- 37S. Salentinig, A. Yaghmur, S. Guillot, O. Glatter, J. Colloid Interface Sci. 2008, 326, 211–220.
- 38D.-H. Kim, S. Lim, J. Shim, J. E. Song, J. S. Chang, K. S. Jin, E. C. Cho, ACS Appl. Mater. Interfaces 2015, 7, 20438–20446.
- 39I. Martiel, L. Sagalowicz, S. Handschin, R. Mezzenga, Langmuir 2014, 30, 14452–14459.
- 40P. T. Spicer, K. L. Hayden, W. Chester, M. L. Lynch, A. Ofori-boateng, J. L. Burns, Langmuir 2001, 17, 5748–5756.
- 41S. B. Rizwan, D. Assmus, A. Boehnke, T. Hanley, B. J. Boyd, T. Rades, S. Hook, Eur. J. Pharm. Biopharm. 2011, 79, 15–22.
- 42J. Barauskas, A. Misiunas, T. Gunnarsson, F. Tiberg, M. Johnsson, Langmuir 2006, 22, 6328–6334.
- 43H. Wang, P. B. Zetterlund, C. Boyer, B. J. Boyd, S. W. Prescott, P. T. Spicer, Soft Matter 2017, 13, 8492–8501.
- 44S. B. Rizwan, W. T. McBurney, K. Young, T. Hanley, B. J. Boyd, T. Rades, S. Hook, J. Controlled Release 2013, 165, 16–21.
- 45H. Kim, C. Leal, ACS Nano 2015, 9, 10214–10226.
- 46Z. Karami, M. Hamidi, Drug Discovery Today 2016, 21, 789–801.
- 47L. Sagalowicz, M. Michel, M. Adrian, P. Frossard, M. Rouvet, H. J. Watzke, A. Yaghmur, L. de Campo, O. Glatter, M. E. Leser, J. Microsc. 2006, 221, 110–121.
- 48J. Zhai, R. Suryadinata, B. Luan, N. Tran, T. Hinton, J. Ratcliffe, X. Hao, C. Drummond, Faraday Discuss. 2016, 191, 545.
- 49S. Murgia, S. Bonacchi, A. M. Falchi, S. Lampis, V. Lippolis, V. Meli, M. Monduzzi, L. Prodi, J. Schmidt, Y. Talmon, et al., Langmuir 2013, 29, 6673–6679.
- 50J. Barauskas, M. Johnsson, F. Joabsson, F. Tiberg, Langmuir 2005, 21, 2569–2577.
- 51S. P. Akhlaghi, I. R. Ribeiro, B. J. Boyd, W. Loh, Colloids Surf. B 2016, 145, 845–853.
- 52F. M. Goñi, A. Alonso, L. A. Bagatolli, R. E. Brown, D. Marsh, M. Prieto, J. L. Thewalt, Biochim. Biophys. Acta Mol. Cell Biol. Lipids 2008, 1781, 665–684.
- 53A. I. I. Tyler, H. M. G. Barriga, E. S. Parsons, N. L. C. McCarthy, O. Ces, R. V. Law, J. M. Seddon, N. J. Brooks, Soft Matter 2015, 11, 3279–3286.
- 54A. Angelova, B. Angelov, V. M. Garamus, P. Couvreur, S. Lesieur, J. Phys. Chem. Lett. 2012, 3, 445–457.
- 55A. Angelova, V. M. Garamus, B. Angelov, Z. Tian, Y. Li, A. Zou, Adv. Colloid Interface Sci. 2017, 249, 331–345.
- 56A. I. I. Tyler, R. V. Law, J. M. Seddon, X-Ray Diffraction of Lipid Model Membranes, Methods in Membrane Lipids, Humana Press, Springer Science+Business Media, New York, 2015, pp. 166–255.
- 57P. P. Wibroe, D. Ahmadvand, M. A. Oghabian, A. Yaghmur, S. M. Moghimi, J. Controlled Release 2016, 221, 1–8.
- 58J. Y. T. Chong, X. Mulet, L. J. Waddington, B. J. Boyd, C. Drummond, Soft Matter 2011, 7, 4768.
- 59B. Angelov, A. Angelova, M. Drechsler, V. M. Garamus, R. Mutafchieva, S. Lesieur, Soft Matter 2015, 11, 3686–3692.
- 60J. Zhai, T. M. Hinton, L. J. Waddington, C. Fong, N. Tran, X. Mulet, C. J. Drummond, B. W. Muir, Langmuir 2015, 31, 10871–10880.
- 61J. Zhai, L. J. Waddington, T. J. Wooster, M.-I. Aguilar, B. J. Boyd, Langmuir 2011, 27, 14757–14766.
- 62J. Y. T. Chong, X. Mulet, B. J. Boyd, C. J. Drummond, in Adv. Planar Lipid Bilayers Liposomes, Academic Press, San Diego, 2015, pp. 131–187.
- 63A. J. Tilley, C. J. Drummond, B. J. Boyd, J. Colloid Interface Sci. 2013, 392, 288–296.
- 64J. L. Grace, N. Alcaraz, N. P. Truong, T. P. Davis, B. J. Boyd, J. F. Quinn, M. R. Whittaker, Chem. Commun. 2017, 53, 10552–10555.
- 65J. Y. T. Chong, X. Mulet, A. Postma, D. J. Keddie, L. J. Waddington, B. J. Boyd, C. Drummond, Soft Matter 2014, 10, 6666–6676.
- 66H. Azhari, M. Strauss, S. Hook, B. J. Boyd, S. B. Rizwan, Eur. J. Pharm. Biopharm. 2016, 104, 148–155.
- 67S. Aleandri, D. Bandera, R. Mezzenga, E. M. Landau, Langmuir 2015, 31, 12770–12776.
- 68J. Zhai, J. A. Scoble, N. Li, G. Lovrecz, L. J. Waddington, N. Tran, B. W. Muir, G. Coia, N. Kirby, C. Drummond, et al., Nanoscale 2015, 7, 2905–2913.
- 69H. H. Shen, V. Lake, A. P. Le Brun, M. James, A. P. Duff, Y. Peng, K. M. McLean, P. G. Hartley, Biomaterials 2013, 34, 8361–8369.
- 70N. Alcaraz, Q. Liu, E. Hanssen, A. Johnston, B. J. Boyd, Bioconjugate Chem. 2018, 29, 149–157.
- 71N. Tran, X. Mulet, A. M. Hawley, T. M. Hinton, S. T. Mudie, B. W. Muir, E. C. Giakoumatos, L. J. Waddington, N. M. Kirby, C. J. Drummond, RSC Adv. 2015, 5, 26785–26795.
- 72S. Deshpande, N. Singh, Langmuir 2017, 33, 3509–3516.
- 73N. F. Bouxsein, C. S. McAllister, K. K. Ewert, C. E. Samuel, C. R. Safinya, Biochemistry 2007, 46, 4785–4792.
- 74T. M. Hinton, F. Grusche, D. Acharya, R. Shukla, V. Bansal, L. J. Waddington, P. Monaghan, B. W. Muir, Toxicol. Res. 2014, 3, 11–22.
- 75J. Barauskas, C. Cervin, M. Jankunec, M. Špandyreva, K. Ribokaitė, F. Tiberg, M. Johnsson, Int. J. Pharm. 2010, 391, 284–291.
- 76S. Murgia, A. M. Falchi, M. Mano, S. Lampis, R. Angius, A. M. Carnerup, J. Schmidt, G. Diaz, M. Giacca, Y. Talmon, et al., J. Phys. Chem. B 2010, 114, 3518–3525.
- 77H. H. Shen, J. G. Crowston, F. Huber, S. Saubern, K. M. McLean, P. G. Hartley, Biomaterials 2010, 31, 9473–9481.
- 78T. E. Hartnett, K. Ladewig, A. J. O'Connor, P. G. Hartley, K. M. McLean, RSC Adv. 2015, 5, 26543–26549.
- 79J. Zhai, N. Tran, S. Sarkar, C. Fong, X. Mulet, C. J. Drummond, Langmuir 2017, 33, 2571–2580.
- 80V. Cherezov, J. Clogston, Y. Misquitta, W. Abdel-Gawad, M. Caffrey, Biophys. J. 2002, 83, 3393–3407.
- 81R. Negrini, R. Mezzenga, Langmuir 2012, 28, 16455–16462.
- 82A. Angelova, B. Angelov, R. Mutafchieva, V. M. Garamus, S. Lesieur, S. S. Funari, R. Willumeit, P. Couvreur, in Trends Colloid Interface Sci. XXIV. Prog. Colloid Polym. Sci., Vol. 138, Springer, Berlin, Heidelberg, 2011, pp. 1–6.
- 83A. Zabara, R. Mezzenga, Soft Matter 2012, 8, 6535–6541.
- 84B. Angelov, A. Angelova, M. Ollivon, C. Bourgaux, A. Campitelli, J. Am. Chem. Soc. 2003, 125, 7188–7189.
- 85H. Kim, Z. Song, C. Leal, Proc. Natl. Acad. Sci. USA 2017, 114, 10834–10839.
- 86A. Zabara, J. Y. T. Chong, I. Martiel, L. Stark, B. A. Cromer, C. Speziale, C. J. Drummond, R. Mezzenga, Nat. Commun. 2018, 9, 544.
- 87H. M. G. Barriga, A. I. I. Tyler, N. L. C. McCarthy, E. S. Parsons, O. Ces, R. V. Law, J. M. Seddon, N. J. Brooks, Soft Matter 2015, 11, 600–607.
- 88R. Bruinsma, J. Phys. II 1992, 425–451.
- 89W. Sun, J. J. Vallooran, W.-K. Fong, R. Mezzenga, J. Phys. Chem. Lett. 2016, 7, 1507–1512.
- 90W. Sun, J. J. Vallooran, A. Zabara, R. Mezzenga, Nanoscale 2014, 6, 6853–6859.
- 91C. Leal, N. F. Bouxsein, K. K. Ewert, C. R. Safinya, J. Am. Chem. Soc. 2010, 132, 16841–16847.
- 92L. van't Hag, S. L. Gras, C. E. Conn, C. J. Drummond, Chem. Soc. Rev. 2017, 46, 2705–2731.
- 93N. Tran, X. Mulet, A. M. Hawley, C. Fong, J. Zhai, T. U. Le, J. Ratcliffe, C. J. Drummond, Langmuir 2018, 34, 2764–2773.
- 94M. Younus, R. N. Prentice, A. N. Clarkson, B. J. Boyd, S. B. Rizwan, Langmuir 2016, 32, 8942–8950.
- 95M. Rittman, M. Frischherz, F. Burgmann, P. G. Hartley, A. Squires, Soft Matter 2010, 6, 4048–4061.
- 96J. J. Vallooran, S. Handschin, S. M. Pillai, B. N. Vetter, S. Rusch, H. Beck, R. Mezzenga, Adv. Funct. Mater. 2015, 26, 181–190.
- 97C. V. Kulkarni, A. Yaghmur, M. Steinhart, M. Kreichbaum, M. Rappolt, Langmuir 2016, 32, 11907–11917.
- 98C. Brasnett, G. Longstaff, L. Compton, A. M. Seddon, Sci. Rep. 2017, 7, 8229.
- 99B. W. Muir, G. Zhen, P. Gunatillake, P. G. Hartley, J. Phys. Chem. B 2012, 116, 3551–3556.
- 100A. Ghazal, M. Gontsarik, J. Kutter, J. P. Lafleur, A. Labrador, K. Mortensen, A. Yaghmur, J. Appl. Crystallogr. 2016, 49, 2005–2014.
- 101A. Yaghmur, B. Sartori, M. Rappolt, Phys. Chem. Chem. Phys. 2011, 13, 3115–3125.
- 102Q. Liu, Y. D. Dong, T. L. Hanley, B. J. Boyd, Langmuir 2013, 29, 14265–14273.
- 103V. Meli, C. Caltagirone, A. M. Falchi, S. T. Hyde, V. Lippolis, M. Monduzzi, M. Obiols-Rabasa, A. Rosa, J. Schmidt, Y. Talmon, et al., Langmuir 2015, 31, 9566–9575.
- 104Y. S. R. Elnaggar, S. M. Etman, D. A. Abdelmonsif, O. Y. Abdallah, Int. J. Nanomed. 2015, 10, 5459–5473.
- 105E. Nazaruk, A. Majkowska-Pilip, R. Bilewicz, ChemPlusChem 2017, 82, 570–575.
- 106C. V. Kulkarni, V. K. Vishwapathi, A. Quarshie, Z. Moinuddin, J. Page, P. Kendrekar, S. S. Mashele, Langmuir 2017, 33, 9907–9915.
- 107T. G. Meikle, A. Zabara, L. J. Waddington, F. Separovic, C. J. Drummond, C. E. Conn, Colloids Surf. B 2017, 152, 143–151.
- 108L. Boge, A. Umerska, N. Matougui, H. Bysell, L. Ringstad, M. Davoudi, J. Eriksson, K. Edwards, M. Andersson, Int. J. Pharm. 2017, 526, 400–412.
- 109Z. Liu, L. Luo, S. Zheng, Y. Niu, R. Bo, Y. Huang, J. Xing, Z. Li, D. Wang, Int. J. Nanomed. 2016, 11, 3571–3583.
- 110B. Angelov, A. Angelova, S. K. Filippov, M. Drechsler, P. Štěpánek, S. Lesieur, ACS Nano 2014, 8, 5216–5226.
- 111B. J. Boyd, Int. J. Pharm. 2003, 260, 239–247.
- 112S. P. Akhlaghi, W. Loh, Eur. J. Pharm. Biopharm. 2017, 117, 60–67.
- 113C. E. Conn, X. Mulet, M. J. Moghaddam, C. Darmanin, L. J. Waddington, S. M. Sagnella, N. Kirby, J. N. Varghese, C. Drummond, Soft Matter 2011, 7, 567–578.
- 114A. Zabara, R. Negrini, O. Onaca-Fischer, R. Mezzenga, Small 2013, 9, 3602–3609.
- 115X. Che, Z. Wang, Y. Liu, Y. Sun, H. Liu, RSC Adv. 2016, 6, 114676–114684.
- 116J. Barauskas, H. Anderberg, A. Svendsen, T. Nylander, Colloids Surf. B 2016, 137, 50–59.
- 117M. Wadsäter, J. Barauskas, T. Nylander, F. Tiberg, ACS Appl. Mater. Interfaces 2014, 6, 7063–7069.
- 118M. Kang, C. Leal, Adv. Funct. Mater. 2016, 26, 5610–5620.
- 119G. Zhen, T. M. Hinton, B. W. Muir, S. Shi, M. Tizard, K. M. McLean, P. G. Hartley, P. Gunatillake, Mol. Pharm. 2012, 9, 2450–2457.
- 120B. Tajik-Ahmadabad, A. Mechler, B. W. Muir, K. McLean, T. M. Hinton, F. Separovic, A. Polyzos, ChemBioChem 2017, 18, 921–930.
- 121M. Kang, H. Kim, C. Leal, Curr. Opin. Colloid Interface Sci. 2016, 26, 58–65.
- 122T. H. Nguyen, C. J. H. Porter, I. Larson, B. J. Boyd, J. Pharm. Pharmacol. 2010, 62, 856–865.
- 123J. Clogston, M. Caffrey, J. Controlled Release 2005, 107, 97–111.
- 124S. Phan, W.-K. Fong, N. Kirby, T. Hanley, B. J. Boyd, Int. J. Pharm. 2011, 421, 176–182.
- 125W.-K. Fong, R. Negrini, J. J. Vallooran, R. Mezzenga, B. J. Boyd, J. Colloid Interface Sci. 2016, 484, 320–339.
- 126M. Kang, G. Huang, C. Leal, Soft Matter 2014, 10, 8846–8854.
- 127R. Negrini, R. Mezzenga, Langmuir 2011, 27, 5296–5303.
- 128M. Szlezak, D. Nieciecka, A. Joniec, M. Pekala, E. Gorecka, M. Emo, M. J. Stébé, P. Krysiński, R. Bilewicz, ACS Appl. Mater. Interfaces 2017, 9, 2796–2805.
- 129M. Kluzek, A. I. I. Tyler, S. Wang, R. Chen, C. M. Marques, F. Thalmann, J. M. Seddon, M. Schmutz, Soft Matter 2017, 13, 7571–7577.
- 130Z. Yang, X. Peng, Y. Tan, M. Chen, X. Zhu, M. Feng, Y. Xu, C. Wu, J. Nanomater. 2011, 308016.
- 131Z. Yang, M. Chen, M. Yang, J. Chen, W. Fang, P. Xu, Int. J. Nanomed. 2014, 9, 327–336.
- 132L. Boge, H. Bysell, L. Ringstad, D. Wennman, A. Umerska, V. Cassisa, J. Eriksson, M. Joly-Gillou, K. Edwards, M. Andersson, Langmuir 2016, 32, 4217–4228.
- 133R. K. Thapa, J. Y. Choi, B. K. Poudel, T. T. Hiep, S. Pathak, B. Gupta, H. Choi, C. S. Yong, J. O. Kim, ACS Appl. Mater. Interfaces 2015, 7, 20360–20368.
- 134M. Nasr, M. K. Ghorab, A. Abdelazem, Acta Pharm. Sin. B 2015, 5, 79–88.
- 135P. Astolfi, E. Giorgini, V. Gambini, B. Rossi, L. Vaccari, F. Vita, O. Francescangeli, C. Marchini, M. Pisani, Langmuir 2017, 33, 12369–12378.
- 136T. Rattanapak, J. Birchall, K. Young, M. Ishii, I. Meglinski, T. Rades, S. Hook, J. Controlled Release 2013, 172, 894–903.
- 137N. M. Morsi, G. A. Abdelbary, M. A. Ahmed, Eur. J. Pharm. Biopharm. 2014, 86, 178–189.
- 138S. Salah, A. A. Mahmoud, A. O. Kamel, Drug Delivery 2017, 24, 846–856.
- 139X. Peng, Y. Zhou, K. Han, L. Qin, L. Dian, G. Li, X. Pan, C. Wu, Drug Des. Dev. Ther. 2015, 9, 4209–4218.
- 140J. Huang, T. Peng, Y. Li, Z. Zhan, Y. Zeng, Y. Huang, X. Pan, C.-Y. Wu, C. Wu, AAPS Pharmscitech 2017, 18, 2919–2926.
- 141R. Liu, S. Wang, S. Fang, J. Wang, J. Chen, X. Huang, X. He, C. Liu, Nanoscale Res. Lett. 2016, 11, 254.
- 142R. Cortesi, M. Campioni, L. Ravani, M. Drechsler, M. Pinotti, E. Esposito, N. Biotechnol. 2014, 31, 44–54.
- 143A. Rosa, S. Murgia, D. Putzu, V. Meli, A. M. Falchi, Chem. Phys. Lipids 2015, 191, 96–105.
- 144A. M. Falchi, A. Rosa, A. Atzeri, A. Incani, S. Lampis, V. Meli, C. Caltagirone, S. Murgia, Toxicol. Res. 2015, 4, 1025–1036.
- 145S. J. Fraser, X. Mulet, L. Martin, S. Praporski, A. Mechler, P. G. Hartley, A. Polyzos, F. Separovic, Langmuir 2012, 28, 620–627.
- 146B. W. Muir, D. P. Acharya, D. F. Kennedy, X. Mulet, R. A. Evans, S. M. Pereira, K. L. Wark, B. J. Boyd, T. H. Nguyen, T. M. Hinton, et al., Biomaterials 2012, 33, 2723–2733.
- 147S. Biffi, C. Andolfi, C. Caltagirone, C. Garrovo, A. M. Falchi, V. Lippolis, A. Lorenzon, P. Macor, V. Meli, M. Monduzzi, Nanotechnology 2017, 28, 055102.
- 148N. Tran, N. Bye, B. A. Moffat, D. K. Wright, A. Cuddihy, T. M. Hinton, A. M. Hawley, N. P. Reynolds, L. J. Waddington, X. Mulet, et al., Mater. Sci. Eng. C 2017, 71, 584–593.
- 149S. Murgia, A. M. Falchi, V. Meli, K. Schillén, V. Lippolis, M. Monduzzi, A. Rosa, J. Schmidt, Y. Talmon, R. Bizzarri, et al., Colloids Surfaces B 2015, 129, 87–94.
- 150V. Cherezov, Curr. Opin. Struct. Biol. 2011, 21, 559–566.