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Current Drug Delivery

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ISSN (Print): 1567-2018
ISSN (Online): 1875-5704

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Review Article

Liposomes for Enhanced Cellular Uptake of Anticancer Agents

Author(s): Gamal M. El Maghraby* and Mona F. Arafa

Volume 17, Issue 10, 2020

Page: [861 - 873] Pages: 13

DOI: 10.2174/1567201817666200708113131

Price: $65

Abstract

Cancers are life threatening diseases and their traditional treatment strategies have numerous limitations which include poor pharmacokinetic profiles, non-specific drug distribution in the body tissues and organs and deprived tumor cells penetration. This attracted the attention of researchers to tailor efficient drug delivery system for anticancer agents to overcome these limitations. Liposomes are one of the newly developed delivery systems for anticancer agents. They are vesicular structures, which were fabricated to enhance drug targeting to tumor tissues either via active or passive targeting. They can be tailored to penetrate tumor cells membrane which is considered the main rate limiting step in antineoplastic therapy. This resulted in enhancing drug cellular uptake and internalization and increasing drug cytotoxic effect. These modifications were achieved via various approaches which included the use of cell-penetrating peptides, the use of lipid substances that can increase liposome fusogenic properties or increase the cell membrane permeability toward amphiphilic drugs, surface modification or ligand targeted liposomes and immuno-liposomes. The modified liposomes were able to enhance anticancer agent’s cellular uptake and this was reflected in their ability to destroy tumor tissues. This review outlines different approaches employed for liposomes modification for enhancing anticancer agent’s cellular uptake.

Keywords: Liposomes, cellular uptake, cell-penetrating peptides, immuno-liposomes, fusogenic liposomes, anticancer.

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[1]
Olusanya, T.O.B.; Ahmad, R.R.H.; Ibegbu, D.M.; Smith, J.R.; Elkordy, A.A. Liposomal drug delivery systems and anticancer drugs. Molecules, 2018, 23, 907-1-17.
[http://dx.doi.org/10.3390/molecules23040907]
[2]
Iyer, A.K.; Khaled, G.; Fang, J.; Maeda, H. Exploiting the enhanced permeability and retention effect for tumor targeting. Drug Discov. Today, 2006, 11(17-18), 812-818.
[http://dx.doi.org/10.1016/j.drudis.2006.07.005 ] [PMID: 16935749]
[3]
Sharma, G.; Anabousi, S.; Ehrhardt, C.; Ravi Kumar, M.N.V. Liposomes as targeted drug delivery systems in the treatment of breast cancer. J. Drug Target., 2006, 14(5), 301-310.
[http://dx.doi.org/10.1080/10611860600809112 ] [PMID: 16882550]
[4]
Massing, U.; Fuxius, S. Liposomal formulations of anticancer drugs: selectivity and effectiveness. Drug Resist. Updat., 2000, 3(3), 171-177.
[http://dx.doi.org/10.1054/drup.2000.0138 ] [PMID: 11498382]
[5]
Alomrani, A.H.; El Maghraby, G.M.; Alanazi, F.K.; Al-Mohanna, M.A.; Alaiya, A.A.; Alsarra, I.A. Liposomes for enhanced cytotoxic activity of Bleomycin. Drug Dev. Res., 2011, 72, 265-273.
[http://dx.doi.org/10.1002/ddr.20394]
[6]
Miyaki, M.; Ono, T.; Hori, S.; Umezawa, H. Binding of bleomycin to DNA in bleomycin-sensitive and -resistant rat ascites hepatoma cells. Cancer Res., 1975, 35(8), 2015-2019.
[PMID: 50129]
[7]
de Graaf, D.; Sharma, R.C.; Mechetner, E.B.; Schimke, R.T.; Roninson, I.B. P-glycoprotein confers methotrexate resistance in 3T6 cells with deficient carrier-mediated methotrexate uptake. Proc. Natl. Acad. Sci. USA, 1996, 93(3), 1238-1242.
[http://dx.doi.org/10.1073/pnas.93.3.1238 ] [PMID: 8577747]
[8]
Heller, R.; Jaroszeski, M.J.; Reintgen, D.S.; Puleo, C.A.; DeConti, R.C.; Gilbert, R.A.; Glass, L.F. Treatment of cutaneous and subcutaneous tumors with electrochemotherapy using intralesional bleomycin. Cancer, 1998, 83(1), 148-157.
[http://dx.doi.org/10.1002/(SICI)1097-0142(19980701)83:1<148::AID CNCR20>3.0.CO;2-W ] [PMID: 9655305]
[9]
Li, H.J.; Du, J.Z.; Du, X.J.; Xu, C.F.; Sun, C.Y.; Wang, H.X.; Cao, Z.T.; Yang, X.Z.; Zhu, Y.H.; Nie, S.; Wang, J. Stimuli-responsive clustered nanoparticles for improved tumor penetration and therapeutic efficacy. Proc. Natl. Acad. Sci. USA, 2016, 113(15), 4164-4169.
[http://dx.doi.org/10.1073/pnas.1522080113 ] [PMID: 27035960]
[10]
Wu, H.; Yu, M.; Miao, Y.; He, S.; Dai, Z.; Song, W.; Liu, Y.; Song, S.; Ahmad, E.; Wang, D.; Gan, Y. Cholesterol-tuned liposomal membrane rigidity directs tumor penetration and anti-tumor effect. Acta Pharm. Sin. B, 2019, 9(4), 858-870.
[http://dx.doi.org/10.1016/j.apsb.2019.02.010 ] [PMID: 31384544]
[11]
Kaur, S.; Kumar, S.; Momi, N.; Sasson, A.R.; Batra, S.K. Mucins in pancreatic cancer and its microenvironment. Nat. Rev. Gastroenterol. Hepatol., 2013, 10(10), 607-620.
[http://dx.doi.org/10.1038/nrgastro.2013.120 ] [PMID: 23856888]
[12]
Levental, K.R.; Yu, H.; Kass, L.; Lakins, J.N.; Egeblad, M.; Erler, J.T.; Fong, S.F.; Csiszar, K.; Giaccia, A.; Weninger, W.; Yamauchi, M.; Gasser, D.L.; Weaver, V.M. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell, 2009, 139(5), 891-906.
[http://dx.doi.org/10.1016/j.cell.2009.10.027 ] [PMID: 19931152]
[13]
Curry, F.E. Drug delivery: redefining tumour vascular barriers. Nat. Nanotechnol., 2016, 11(6), 494-496.
[http://dx.doi.org/10.1038/nnano.2016.21 ] [PMID: 26878144]
[14]
Li, X.; Ding, L.; Xu, Y.; Wang, Y.; Ping, Q. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int. J. Pharm., 2009, 373(1-2), 116-123.
[http://dx.doi.org/10.1016/j.ijpharm.2009.01.023 ] [PMID: 19429296]
[15]
Deshpande, P.P.; Biswas, S.; Torchilin, V.P. Current trends in the use of liposomes for tumor targeting. Nanomedicine (Lond.), 2013, 8(9), 1509-1528.
[http://dx.doi.org/10.2217/nnm.13.118 ] [PMID: 23914966]
[16]
Sihorkar, V.; Vyas, S.P. Potential of polysaccharide anchored liposomes in drug delivery, targeting and immunization. J. Pharm. Pharm. Sci., 2001, 4(2), 138-158.
[PMID: 11466172]
[17]
Riaz, M.K.; Riaz, M.A. Zhang, Xue.; Lin, C.; Wong, K.H.; Chen, X.; Z, G.; ILu, A.; Yang, Z. Surface functionalization and targeting strategies of liposomes in solid tumor therapy: a review. Int. J. Mol. Sci., 2018, 19(195), 1-27.
[18]
Hong, R.L.; Huang, C.J.; Tseng, Y.L.; Pang, V.F.; Chen, S.T.; Liu, J.J.; Chang, F.H. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in C-26 tumor-bearing mice: is surface coating with polyethylene glycol beneficial? Clin. Cancer Res., 1999, 5(11), 3645-3652.
[PMID: 10589782]
[19]
Ng, K.; Zhao, L.; Liu, Y.; Mahapatro, M. The effects of polyethyleneglycol (PEG)-derived lipid on the activity of target-sensitive immunoliposome. Int. J. Pharm., 2000, 193(2), 157-166.
[http://dx.doi.org/10.1016/S0378-5173(99)00330-0 ] [PMID: 10606778]
[20]
Lewin, M.; Carlesso, N.; Tung, C.H.; Tang, X.W.; Cory, D.; Scadden, D.T.; Weissleder, R. Tat peptide-derivatized magnetic nanoparticles allow in vivo tracking and recovery of progenitor cells. Nat. Biotechnol., 2000, 18(4), 410-414.
[http://dx.doi.org/10.1038/74464 ] [PMID: 10748521]
[21]
Green, M.; Loewenstein, P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell, 1988, 55(6), 1179-1188.
[http://dx.doi.org/10.1016/0092-8674(88)90262-0 ] [PMID: 2849509]
[22]
Torchilin, V.P.; Rammohan, R.; Weissig, V.; Levchenko, T.S. TAT peptide on the surface of liposomes affords their efficient intracellular delivery even at low temperature and in the presence of metabolic inhibitors. Proc. Natl. Acad. Sci. USA, 2001, 98(15), 8786-8791.
[http://dx.doi.org/10.1073/pnas.151247498 ] [PMID: 11438707]
[23]
Tseng, Y.L.; Liu, J.J.; Hong, R.L. Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: a kinetic and efficacy study. Mol. Pharmacol., 2002, 62(4), 864-872.
[http://dx.doi.org/10.1124/mol.62.4.864 ] [PMID: 12237333]
[24]
Fretz, M.M.; Koning, G.A.; Mastrobattista, E.; Jiskoot, W.; Storm, G. OVCAR-3 cells internalize TAT-peptide modified liposomes by endocytosis. Biochim. Biophys. Acta, 2004, 1665(1-2), 48-56.
[http://dx.doi.org/10.1016/j.bbamem.2004.06.022 ] [PMID: 15471570]
[25]
Ran, R.; Zhang, L.; Tang, J.; Yin, Y.J.; Qin, Y.; Liu, Y.Y.; Zhang, Z.R.; He, Q. Enhanced tumor accumulation and cellular uptake of liposomes modified with ether-bond linked cholesterol derivatives. Pharmazie, 2013, 68(8), 668-674.
[PMID: 24020121]
[26]
Kim, C.K.; Lim, S.J. Liposome Immunoassay (LIA) with antigen-coupled liposomes containing alkaline phosphatase. J. Immunol. Methods, 1993, 159(1-2), 101-106.
[http://dx.doi.org/10.1016/0022-1759(93)90146-X ] [PMID: 8445242]
[27]
Chen, Z.; Deng, J.; Zhao, Y.; Tao, T. Cyclic RGD peptide-modified liposomal drug delivery system: enhanced cellular uptake in vitro and improved pharmacokinetics in rats. Int. J. Nanomedicine, 2012, 7, 3803-3811.
[http://dx.doi.org/10.2147/IJN.S33541 ] [PMID: 22888235]
[28]
Song, Z.; Lin, Y.; Zhang, X.; Feng, C.; Lu, Y.; Gao, Y.; Dong, C. Cyclic RGD peptide-modified liposomal drug delivery system for targeted oral apatinib administration: enhanced cellular uptake and improved therapeutic effects. Int. J. Nanomedicine, 2017, 12, 1941-1958.
[http://dx.doi.org/10.2147/IJN.S125573 ] [PMID: 28331317]
[29]
Liu, Y.; Ji, M.; Wong, M.K.; Joo, K.I.; Wang, P. Enhanced therapeutic efficacy of iRGD-conjugated crosslinked multilayer liposomes for drug delivery. BioMed Res. Int., 2013, 2013, 378380.
[http://dx.doi.org/10.1155/2013/378380 ] [PMID: 23691500]
[30]
Nik, M.E.; Malaekeh-Nikouei, B.; Amin, M.; Hatamipour, M.; Teymouri, M.; Sadeghnia, H.R.; Iranshahi, M.; Jaafari, M.R. Liposomal formulation of Galbanic acid improved therapeutic efficacy of pegylated liposomal doxorubicin in mouse colon carcinoma. Sci. Rep., 2019, 9(1), 9527.
[http://dx.doi.org/10.1038/s41598-019-45974-7 ] [PMID: 31267009]
[31]
El-Sayed, A.; Khalil, I.A.; Kogure, K.; Futaki, S.; Harashima, H. Octaarginine- and octalysine-modified nanoparticles have different modes of endosomal escape. J. Biol. Chem., 2008, 283(34), 23450-23461.
[http://dx.doi.org/10.1074/jbc.M709387200 ] [PMID: 18550548]
[32]
Sawant, R.; Torchilin, V. Intracellular delivery of nanoparticles with CPPs. Methods Mol. Biol., 2011, 683, 431-451.
[http://dx.doi.org/10.1007/978-1-60761-919-2_31 ] [PMID: 21053148]
[33]
Koshkaryev, A.; Piroyan, A.; Torchilin, V.P. Bleomycin in octaarginine-modified fusogenic liposomes results in improved tumor growth inhibition. Cancer Lett., 2013, 334(2), 293-301.
[http://dx.doi.org/10.1016/j.canlet.2012.06.008 ] [PMID: 22743614]
[34]
Biswas, S.; Dodwadkar, N.S.; Deshpande, P.P.; Parab, S.; Torchilin, V.P. Surface functionalization of doxorubicin-loaded liposomes with octa-arginine for enhanced anticancer activity. Eur. J. Pharm. Biopharm., 2013, 84(3), 517-525.
[http://dx.doi.org/10.1016/j.ejpb.2012.12.021 ] [PMID: 23333899]
[35]
Jang, J.H.; Kim, Y.J.; Kim, H.; Kim, S.C.; Cho, J.H. Buforin IIb induces endoplasmic reticulum stress-mediated apoptosis in HeLa cells. Peptides, 2015, 69, 144-149.
[http://dx.doi.org/10.1016/j.peptides.2015.04.024 ] [PMID: 25958204]
[36]
Lim, K.J.; Sung, B.H.; Shin, J.R.; Lee, Y.W.; Kim, D.J.; Yang, K.S.; Kim, S.C. A cancer specific cell-penetrating peptide, BR2, for the efficient delivery of an scFv into cancer cells. PLoS One, 2013, 8(6), e66084.
[http://dx.doi.org/10.1371/journal.pone.0066084 ] [PMID: 23776609]
[37]
Zhang, X.; Lin, C.; Lu, A.; Lin, G.; Chen, H.; Liu, Q.; Yang, Z.; Zhang, H. Liposomes equipped with cell penetrating peptide BR2 enhances chemotherapeutic effects of cantharidin against hepatocellular carcinoma. Drug Deliv., 2017, 24(1), 986-998.
[http://dx.doi.org/10.1080/10717544.2017.1340361 ] [PMID: 28644728]
[38]
Weitman, S.D.; Weinberg, A.G.; Coney, L.R.; Zurawski, V.R.; Jennings, D.S.; Kamen, B.A. Cellular localization of the folate receptor: potential role in drug toxicity and folate homeostasis. Cancer Res., 1992, 52(23), 6708-6711.
[PMID: 1330299]
[39]
Antony, A.C. Megaloblastic anemias.Hematology: Basic principles and practice. HoVman, R.; Ed.; New York: Churchill-Livingstone, 2000, pp. 446-485.
[40]
Kamen, B.A. Folate receptors. Folate and human development. Massaro, E.J; Rogers, J.M., Ed.; Humana Press: Totowa, NJ, 2002, pp. 117-135.
[http://dx.doi.org/10.1385/1-59259-164-7:117]
[41]
Matherly, L.H.; Goldman, D.I. Membrane transport of folates. Vitam. Horm., 2003, 66, 403-456.
[http://dx.doi.org/10.1016/S0083-6729(03)01012-4 ] [PMID: 12852262]
[42]
Pillai, M.R.; Chacko, P.; Kesari, L.A.; Jayaprakash, P.G.; Jayaram, H.N.; Antony, A.C. Expression of folate receptors and heterogeneous nuclear ribonucleoprotein E1 in women with human papillomavirus mediated transformation of cervical tissue to cancer. J. Clin. Pathol., 2003, 56(8), 569-574.
[http://dx.doi.org/10.1136/jcp.56.8.569 ] [PMID: 12890803]
[43]
Gupta, Y.; Jain, A.; Jain, P.; Jain, S.K. Design and development of folate appended liposomes for enhanced delivery of 5-FU to tumor cells. J. Drug Target., 2007, 15(3), 231-240.
[http://dx.doi.org/10.1080/10611860701289719 ] [PMID: 17454361]
[44]
Bothun, G.D.; Lelis, A.; Chen, Y.; Scully, K.; Anderson, L.E.; Stoner, M.A. Multicomponent folate-targeted magnetoliposomes: design, characterization, and cellular uptake. Nanomedicine (Lond.), 2011, 7(6), 797-805.
[http://dx.doi.org/10.1016/j.nano.2011.02.007 ] [PMID: 21419872]
[45]
Lu, Y.; Ding, N.; Yang, C.; Huang, L.; Liu, J.; Xiang, G. Preparation and in vitro evaluation of a folate-linked liposomal curcumin formulation. J. Liposome Res., 2012, 22(2), 110-119.
[http://dx.doi.org/10.3109/08982104.2011.627514 ] [PMID: 22372871]
[46]
Jadia, R.; Kydd, J.; Piel, B.; Rai, P. Liposomes aid curcumin’s combat with cancer in a breast tumor model. Oncomedicine, 2018, 3, 94-109.
[http://dx.doi.org/10.7150/oncm.27938]
[47]
Qian, Z.M.; Li, H.; Sun, H.; Ho, K. Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway. Pharmacol. Rev., 2002, 54(4), 561-587.
[http://dx.doi.org/10.1124/pr.54.4.561 ] [PMID: 12429868]
[48]
Ishida, O.; Maruyama, K.; Tanahashi, H.; Iwatsuru, M.; Sasaki, K.; Eriguchi, M.; Yanagie, H. Liposomes bearing polyethyleneglycol-coupled transferrin with intracellular targeting property to the solid tumors in vivo. Pharm. Res., 2001, 18(7), 1042-1048.
[http://dx.doi.org/10.1023/A:1010960900254 ] [PMID: 11496943]
[49]
Furumoto, K.; Yokoe, J.; Ogawara, K.; Amano, S.; Takaguchi, M.; Higaki, K.; Kai, T.; Kimura, T. Effect of coupling of albumin onto surface of PEG liposome on its in vivo disposition. Int. J. Pharm., 2007, 329(1-2), 110-116.
[http://dx.doi.org/10.1016/j.ijpharm.2006.08.026 ] [PMID: 17000067]
[50]
Yokoe, J.; Sakuragi, S.; Yamamoto, K.; Teragaki, T.; Ogawara, K.; Higaki, K.; Katayama, N.; Kai, T.; Sato, M.; Kimura, T. Albumin-conjugated PEG liposome enhances tumor distribution of liposomal doxorubicin in rats. Int. J. Pharm., 2008, 353(1-2), 28-34.
[http://dx.doi.org/10.1016/j.ijpharm.2007.11.008 ] [PMID: 18082345]
[51]
Clarke, J.; Itzhaki, L.S. Hydrogen exchange and protein folding. Curr. Opin. Struct. Biol., 1998, 8(1), 112-118.
[http://dx.doi.org/10.1016/S0959-440X(98)80018-3 ] [PMID: 9519304]
[52]
Jung, S.H.; Kim, S.K.; Jung, S.H.; Kim, E.H.; Cho, S.H.; Jeong, K.S.; Seong, H.; Shin, B.C. Increased stability in plasma and enhanced cellular uptake of thermally denatured albumin-coated liposomes. Colloids Surf. B Biointerfaces, 2010, 76(2), 434-440.
[http://dx.doi.org/10.1016/j.colsurfb.2009.12.002 ] [PMID: 20036109]
[53]
Nettles, D.L.; Chilkoti, A.; Setton, L.A. Applications of elastin-like polypeptides in tissue engineering. Adv. Drug Deliv. Rev., 2010, 62(15), 1479-1485.
[http://dx.doi.org/10.1016/j.addr.2010.04.002 ] [PMID: 20385185]
[54]
Na, K.; Lee, S.A.; Jung, S.H.; Hyun, J.; Shin, B.C. Elastin-like polypeptide modified liposomes for enhancing cellular uptake into tumor cells. Colloids Surf. B Biointerfaces, 2012, 91, 130-136.
[http://dx.doi.org/10.1016/j.colsurfb.2011.10.051 ] [PMID: 22104404]
[55]
Wang, W.; Shao, A.; Zhang, N.; Fang, J.; Ruan, J.J.; Ruan, B.H. Cationic polymethacrylate-modified liposomes significantly enhanced doxorubicin delivery and antitumor activity. Sci. Rep., 2017, 7, 43036.
[http://dx.doi.org/10.1038/srep43036 ] [PMID: 28225062]
[56]
Mu, C.F.; Balakrishnan, P.; Cui, F.D.; Yin, Y.M.; Lee, Y.B.; Choi, H.G.; Yong, C.S.; Chung, S.J.; Shim, C.K.; Kim, D.D. The effects of mixed MPEG-PLA/Pluronic copolymer micelles on the bioavailability and multidrug resistance of docetaxel. Biomaterials, 2010, 31(8), 2371-2379.
[http://dx.doi.org/10.1016/j.biomaterials.2009.11.102 ] [PMID: 20031202]
[57]
Minko, T.; Batrakova, E.V.; Li, S.; Li, Y.; Pakunlu, R.I.; Alakhov, V.Y.; Kabanov, A.V. Pluronic block copolymers alter apoptotic signal transduction of doxorubicin in drug-resistant cancer cells. J. Control. Release, 2005, 105(3), 269-278.
[http://dx.doi.org/10.1016/j.jconrel.2005.03.019 ] [PMID: 15939500]
[58]
Song, C.K.; Balakrishnan, P.; Shim, C.K.; Chung, S.J.; Kim, D.D. Enhanced in vitro cellular uptake of P-gp substrate by Poloxamer-Modified Liposomes (PMLs) in MDR cancer cells. J. Microencapsul., 2011, 28(6), 575-581.
[http://dx.doi.org/10.3109/02652048.2011.599436 ] [PMID: 21770706]
[59]
Muthu, M.S.; Kulkarni, S.A.; Xiong, J.; Feng, S.S. Vitamin E TPGS coated liposomes enhanced cellular uptake and cytotoxicity of docetaxel in brain cancer cells. Int. J. Pharm., 2011, 421(2), 332-340.
[http://dx.doi.org/10.1016/j.ijpharm.2011.09.045 ] [PMID: 22001537]
[60]
Li, T.; Takeoka, S. A novel application of maleimide for advanced drug delivery: in vitro and in vivo evaluation of maleimide-modified pH-sensitive liposomes. Int. J. Nanomedicine, 2013, 8, 3855-3866.
[PMID: 24143089]
[61]
Li, T.; Takeoka, S. Enhanced cellular uptake of maleimide-modified liposomes via thiol-mediated transport. Int. J. Nanomedicine, 2014, 9, 2849-2861.
[PMID: 24940060]
[62]
Li, Y.; Cheng, Q.; Jiang, Q.; Huang, Y.; Liu, H.; Zhao, Y.; Cao, W.; Ma, G.; Dai, F.; Liang, X.; Liang, Z.; Zhang, X. Enhanced endosomal/lysosomal escape by distearoyl phosphoethanolamine-polycarboxybetaine lipid for systemic delivery of siRNA. J. Control. Release, 2014, 176, 104-114.
[http://dx.doi.org/10.1016/j.jconrel.2013.12.007 ] [PMID: 24365128]
[63]
Li, Y.; Liu, R.; Yang, J.; Shi, Y.; Ma, G.; Zhang, Z.; Zhang, X. Enhanced retention and anti-tumor efficacy of liposomes by changing their cellular uptake and pharmacokinetics behavior. Biomaterials, 2015, 41, 1-14.
[http://dx.doi.org/10.1016/j.biomaterials.2014.11.010 ] [PMID: 25522960]
[64]
Maekawa-Matsuura, M.; Fujieda, K.; Maekawa, Y.; Nishimura, T.; Nagase, K.; Kanazawa, H. LAT1-targeting thermoresponsive liposomes for effective cellular uptake by cancer cells. ACS Omega, 2019, 4, 6443-6451.
[http://dx.doi.org/10.1021/acsomega.9b00216]
[65]
Park, J.W.; Hong, K.; Kirpotin, D.B.; Colbern, G.; Shalaby, R.; Baselga, J.; Shao, Y.; Nielsen, U.B.; Marks, J.D.; Moore, D.; Papahadjopoulos, D.; Benz, C.C. Anti-HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res., 2002, 8(4), 1172-1181.
[PMID: 11948130]
[66]
ElBayoumi, T.A.; Torchilin, V.P. Tumor-targeted nanomedicines: enhanced antitumor efficacy in vivo of doxorubicin-loaded, long-circulating liposomes modified with cancer-specific monoclonal antibody. Clin. Cancer Res., 2009, 15(6), 1973-1980.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-2392 ] [PMID: 19276264]
[67]
Mamot, C.; Drummond, D.C.; Greiser, U.; Hong, K.; Kirpotin, D.B.; Marks, J.D.; Park, J.W. Epidermal Growth Factor Receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFR- and EGFRvIII-overexpressing tumor cells. Women’s Oncol. Rev., 2004, 4, 99-101.
[http://dx.doi.org/10.3109/14733400410001727592]
[68]
Balzar, M.; Winter, M.J.; de Boer, C.J.; Litvinov, S.V. The biology of the 17-1A antigen (Ep-CAM). J. Mol. Med. (Berl.), 1999, 77(10), 699-712.
[http://dx.doi.org/10.1007/s001099900038 ] [PMID: 10606205]
[69]
Hussain, S.; Plückthun, A.; Allen, T.M.; Zangemeister-Wittke, U. Chemosensitization of carcinoma cells using epithelial cell adhesion molecule-targeted liposomal antisense against bcl-2/bcl-xL. Mol. Cancer Ther., 2006, 5(12), 3170-3180.
[http://dx.doi.org/10.1158/1535-7163.MCT-06-0412 ] [PMID: 17172421]
[70]
Hatakeyama, H.; Akita, H.; Ishida, E.; Hashimoto, K.; Kobayashi, H.; Aoki, T.; Yasuda, J.; Obata, K.; Kikuchi, H.; Ishida, T.; Kiwada, H.; Harashima, H. Tumor targeting of doxorubicin by anti-MT1-MMP antibody-modified PEG liposomes. Int. J. Pharm., 2007, 342(1-2), 194-200.
[http://dx.doi.org/10.1016/j.ijpharm.2007.04.037 ] [PMID: 17583453]
[71]
Collins, A.T.; Berry, P.A.; Hyde, C.; Stower, M.J.; Maitland, N.J. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res., 2005, 65(23), 10946-10951.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-2018 ] [PMID: 16322242]
[72]
Arabi, L.; Badiee, A.; Mosaffa, F.; Jaafari, M.R. Targeting CD44 expressing cancer cells with anti-CD44 monoclonal antibody improves cellular uptake and antitumor efficacy of liposomal doxorubicin. J. Control. Release, 2015, 220(Pt A), 275-286.
[http://dx.doi.org/10.1016/j.jconrel.2015.10.044] [PMID: 26518722]
[73]
Li, Y.; Cozzi, P.J. MUC1 is a promising therapeutic target for prostate cancer therapy. Curr. Cancer Drug Targets, 2007, 7(3), 259-271.
[http://dx.doi.org/10.2174/156800907780618338 ] [PMID: 17504123]
[74]
Moosavian, S.A.; Abnous, K.; Akhtari, J.; Arabi, L.; Gholamzade Dewin, A.; Jafari, M. 5TR1 aptamer-PEGylated liposomal doxorubicin enhances cellular uptake and suppresses tumour growth by targeting MUC1 on the surface of cancer cells. Artif. Cells Nanomed. Biotechnol., 2018, 46(8), 2054-2065.
[PMID: 29205059]
[75]
Torchilin, V.P.; Zhou, F.; Huang, L. pH-Sensitive liposomes. J. Liposome Res., 1993, 3, 201-255.
[http://dx.doi.org/10.3109/08982109309148213]
[76]
Chu, C.J.; Dijkstra, J.; Lai, M.Z.; Hong, K.; Szoka, F.C. Efficiency of cytoplasmic delivery by pH-sensitive liposomes to cells in culture. Pharm. Res., 1990, 7(8), 824-834.
[http://dx.doi.org/10.1023/A:1015908831507 ] [PMID: 2172955]
[77]
Ghanbarzadeh, S.; Khorrami, A.; Mohamed Khosroshahi, L.; Arami, S. Fusogenic pH sensitive liposomal formulation for rapamycin: improvement of antiproliferative effect. Pharm. Biol., 2014, 52(7), 848-854.
[http://dx.doi.org/10.3109/13880209.2013.871640 ] [PMID: 24920230]
[78]
Koren, E.; Apte, A.; Jani, A.; Torchilin, V.P. Multifunctional PEGylated 2C5-immunoliposomes containing pH-sensitive bonds and TAT peptide for enhanced tumor cell internalization and cytotoxicity. J. Control. Release, 2012, 160(2), 264-273.
[http://dx.doi.org/10.1016/j.jconrel.2011.12.002 ] [PMID: 22182771]
[79]
Apte, A.; Koren, E.; Koshkaryev, A.; Torchilin, V.P. Doxorubicin in TAT peptide-modified multifunctional immunoliposomes demonstrates increased activity against both drug-sensitive and drug-resistant ovarian cancer models. Cancer Biol. Ther., 2014, 15(1), 69-80.
[http://dx.doi.org/10.4161/cbt.26609 ] [PMID: 24145298]
[80]
Veldman, R.J.; Koning, G.A.; van Hell, A.; Zerp, S.; Vink, S.R.; Storm, G.; Verheij, M.; van Blitterswijk, W.J. Coformulated N-octanoyl-glucosylceramide improves cellular delivery and cytotoxicity of liposomal doxorubicin. J. Pharmacol. Exp. Ther., 2005, 315(2), 704-710.
[http://dx.doi.org/10.1124/jpet.105.087486 ] [PMID: 16040815]
[81]
Jia, Y.; Sheng, Z.; Hu, D.; Yan, F.; Zhu, M.; Gao, G.; Wang, P.; Liu, X.; Wang, X.; Zheng, H. Highly penetrative liposome nanomedicine generated by a biomimetic strategy for enhanced cancer chemotherapy. Biomater. Sci., 2018, 6(6), 1546-1555.
[http://dx.doi.org/10.1039/C8BM00256H ] [PMID: 29694474]

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