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Original Research

Effects of Surface Charge, PEGylation and Functionalization with Dipalmitoylphosphatidyldiglycerol on Liposome–Cell Interactions and Local Drug Delivery to Solid Tumors via Thermosensitive Liposomes

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Pages 4045-4061 | Published online: 14 Jun 2021

References

  • Bulbake U, Doppalapudi S, Kommineni N, Khan W. Liposomal formulations in clinical use: an updated review. Pharmaceutics. 2017;9(2):51–59. doi:10.3390/pharmaceutics9020012
  • Douer D. Efficacy and safety of vincristine sulfate liposome injection in the treatment of adult acute lymphocytic leukemia. Oncologist. 2016;21(7):840–847. doi:10.1634/theoncologist.2015-0391
  • O’Brien ME, Wigler N, Inbar M, et al. Reduced cardiotoxicity and comparable efficacy in a Phase III trial of pegylated liposomal doxorubicin HCl (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer. Ann Oncol. 2004;15(3):440–449. doi:10.1093/annonc/mdh097
  • Wang-Gillam A, Li CP, Bodoky G, et al. Nanoliposomal irinotecan with fluorouracil and folinic acid in metastatic pancreatic cancer after previous gemcitabine-based therapy (NAPOLI-1): a global, randomised, open-label, Phase 3 trial. Lancet. 2016;387(10018):545–557. doi:10.1016/S0140-6736(15)00986-1
  • Judson I, Radford JA, Harris M, et al. Randomised Phase II trial of pegylated liposomal doxorubicin (DOXIL/CAELYX) versus doxorubicin in the treatment of advanced or metastatic soft tissue sarcoma: a study by the EORTC Soft Tissue and Bone Sarcoma Group. Eur J Cancer. 2001;37(7):870–877. doi:10.1016/S0959-8049(01)00050-8
  • Laginha KM, Verwoert S, Charrois GJ, Allen TM. Determination of doxorubicin levels in whole tumor and tumor nuclei in murine breast cancer tumors. Cli Cancer Res. 2005;11(19):6944–6949. doi:10.1158/1078-0432.CCR-05-0343
  • Zamboni WC, Gervais AC, Egorin MJ, et al. Systemic and tumor disposition of platinum after administration of cisplatin or STEALTH liposomal-cisplatin formulations (SPI-077 and SPI-077 B103) in a preclinical tumor model of melanoma. Cancer Chemother Pharmacol. 2004;53(4):329–336. doi:10.1007/s00280-003-0719-4
  • Mura S, Nicolas J, Couvreur P. Stimuli-responsive nanocarriers for drug delivery. Nat Mat. 2013;12(11):991–1003. doi:10.1038/nmat3776
  • Kneidl B, Peller M, Winter G, Lindner LH, Hossann M. Thermosensitive liposomal drug delivery systems: state of the art review. Int J Nanomedicine. 2014;16(9):4387–4398.
  • Nardecchia S, Sanchez-Moreno P, Vicente J, Marchal JA, Boulaiz H. Clinical trials of thermosensitive nanomaterials: an overview. Nanomaterials. 2019;9(2):191. doi:10.3390/nano9020191
  • Manzoor AA, Lindner LH, Landon CD, et al. Overcoming limitations in nanoparticle drug delivery: triggered, intravascular release to improve drug penetration into tumors. Cancer Res. 2012;72(21):5566–5575. doi:10.1158/0008-5472.CAN-12-1683
  • Dewhirst MW, Secomb TW. Transport of drugs from blood vessels to tumour tissue. Nat Rev Cancer. 2017;17(12):738–750. doi:10.1038/nrc.2017.93
  • Dicheva BM, ten.Hagen TLM, Li L. Cationic thermosensitive liposomes: a novel dual targeted heat-triggered drug delivery approach for endothelial and tumor cells. Nano Lett. 2013;13(6):2324–2331. doi:10.1021/nl3014154
  • Krasnici S, Werner A, Eichhorn ME, et al. Effect of the surface charge of liposomes on their uptake by angiogenic tumor vessels. Int j Cancer. 2003;105(4):561–567. doi:10.1002/ijc.11108
  • Campbell RB, Brown DF, et al. Cationic charge determines the distribution of liposomes between the vascular and extravascular compartments of tumors. Cancer Res. 2002;62(23):6831–6836.
  • Augustin HA, Braun K, Telemenakis I, Modlich U, Kuhn W. Phenotypic characterization of endothelial cells in a physiological model of blood vessel growth and regression. Am J Pathol. 1995;147(2):339–352.
  • Qu H, Nagy JA, Senger DR, Dvorak HF, Dvorak AM. Ultrastructural localization of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) to the abluminal plasma membrane and vesiculovacuolar organelles of tumor microvascular endothelium. J Histochem Cytochem. 1995;43(4):381–389. doi:10.1177/43.4.7534783
  • Campbell RB, Ying B, Kuesters GM, Hemphill R. Fighting cancer: from the bench to bedside using second generation cationic liposomal therapeutics. J Pharm Sci. 2009;98(2):411–429. doi:10.1002/jps.21458
  • Wu J, Lee A, Lu Y, Lee RJ. Vascular targeting of doxorubicin using cationic liposomes. Int J Pharm. 2007;337(1–2):329–335. doi:10.1016/j.ijpharm.2007.01.003
  • Luo D, Geng J, Li N, et al. Vessel-targeted chemophototherapy with cationic porphyrin-phospholipid liposomes. Mol Cancer Ther. 2017;16(11):2452–2461. doi:10.1158/1535-7163.MCT-17-0276
  • Wang W, Shao A, Zhang N, Fang J, Ruan JJ, Ruan BH. Cationic polymethacrylate-modified liposomes significantly enhanced doxorubicin delivery and antitumor activity. Sci Rep. 2017;7:43036. doi:10.1038/srep43036
  • Strieth S, Eichhorn ME, Sauer B, et al. Neovascular targeting chemotherapy: encapsulation of paclitaxel in cationic liposomes impairs functional tumor microvasculature. Int J Cancer. 2004;110(1):117–124. doi:10.1002/ijc.20083
  • Chonn A, Cullis PR, Devine DV. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J Immunol. 1992;146(12):4234–4241.
  • Knudsen KB, Northeved H, Kumar PE, et al. In vivo toxicity of cationic micelles and liposomes. Nanomedicine. 2015;11(2):467–477. doi:10.1016/j.nano.2014.08.004
  • Lohr JM, Haas SL, Bechstein WO, et al. Cationic liposomal paclitaxel plus gemcitabine or gemcitabine alone in patients with advanced pancreatic cancer: a randomized controlled phase II trial. Ann Oncol. 2012;23(5):1214–1222. doi:10.1093/annonc/mdr379
  • Semple SC, Chonn A, Cullis PR. Interactions of liposomes and lipid-based carrier systems with blood proteins: relation to clearance behaviour in vivo. Adv Drug Deliv Rev. 1988;32(1–2):3–17. doi:10.1016/S0169-409X(97)00128-2
  • Salmaso S, Caliceti P. Stealth properties to improve therapeutic efficacy of drug nanocarriers. J Drug Deliv. 2013;2013:1–19. doi:10.1155/2013/374252
  • Klibanov AL, Maruyama K, Torchilin VP, Huang L. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett. 1990;268(1):237–251. doi:10.1016/0014-5793(90)81016-H
  • Maruyama K, Vuda T, Okamoto A, Kojima S, Suginaka A, lwatsuru M. Prolonged circulation time in vivo of large unilamellar liposomes composed of distearoyl phosphatidylcholine and cholesterol containing amphipathic poly(ethylene glycol). Biochim Biophys Acta. 1992;1128(1):44–49. doi:10.1016/0005-2760(92)90255-T
  • Pozzi D, Colapicchioni V, Caracciolo G, et al. Effect of polyethyleneglycol (PEG) chain length on the bio-nano-interactions between PEGylated lipid nanoparticles and biological fluids: from nanostructure to uptake in cancer cells. Nanoscale. 2014;6(5):2782–2792. doi:10.1039/c3nr05559k
  • Dan N. Effect of liposome charge and PEG polymer layer thickness on cell–liposome electrostatic interactions. Biochim Biophys Acta. 2002;1564(2):343–348. doi:10.1016/S0005-2736(02)00468-6
  • Sanchez L, Yi Y, Yu Y. Effect of partial PEGylation on particle uptake by macrophages. Nanoscale. 2017;9(1):288–297. doi:10.1039/C6NR07353K
  • Degors IMS, Wang C, Rehman ZU, Zuhorn IS. Carriers break barriers in drug delivery: endocytosis and endosomal escape of gene delivery vectors. Acc Chem Res. 2019;52(7):1750–1760. doi:10.1021/acs.accounts.9b00177
  • Lindner LH, Eichhorn ME, Eibl H, et al. Novel temperature-sensitive liposomes with prolonged circulation time. Clin Cancer Res. 2004;10(6):2168–2178. doi:10.1158/1078-0432.CCR-03-0035
  • Hossann M, Wiggenhorn M, Schwerdt A, et al. In vitro stability and content release properties of phosphatidylglyceroglycerol containing thermosensitive liposomes. Biochim Biophys Acta. 2007;1768(10):2491–2499. doi:10.1016/j.bbamem.2007.05.021
  • Limmer S, Hahn J, Schmidt R, et al. Gemcitabine treatment of rat soft tissue sarcoma with phosphatidyldiglycerol-based thermosensitive liposomes. Pharm Res. 2014;31(9):2276–2286. doi:10.1007/s11095-014-1322-6
  • Zimmermann K, Hossann M, Hirschberger J. et al. A pilot trial of doxorubicin containing phosphatidyldiglycerol based thermosensitive liposomes in spontaneous feline soft tissue sarcoma. Int J Hyperthermia;2016. 1–13. doi:10.3109/02656736.2015.1131338
  • Hossann M, Hirschberger J, Schmidt R, et al. A heat-activated drug delivery platform based on phosphatidyl-(oligo)-glycerol nanocarrier for effective cancer treatment. Adv NanoBiomed Res. 2021:200089. doi:10.1002/anbr.202000089.
  • Haran H, Cohen R, Bar LK, Barenholz Y. Transmembrane ammonium sulfate gradients in liposomes produce efficient and stable entrapment of amphipathic weak bases. Biochim Biophys Acta. 1993;1151(2):201–215. doi:10.1016/0005-2736(93)90105-9
  • Eibl H, Lands WEM. A new, sensitive determination of phosphate. Anal Biochem. 1969;30(1):51–57. doi:10.1016/0003-2697(69)90372-8
  • Vichai V, Sulforhodamine KK. B colorimetric assay for cytotoxicity screening. Nat Protoc. 2006;1(3):1112–1116. doi:10.1038/nprot.2006.179
  • Peller M, Willerding L, Limmer S, et al. Surrogate MRI markers for hyperthermia-induced release of doxorubicin from thermosensitive liposomes in tumors. J Control Release. 2016;237:138–146. doi:10.1016/j.jconrel.2016.06.035
  • Lokerse WJM, Lazarian A, Kleinhempel A, et al. Mechanistic investigation of thermosensitive liposome immunogenicity and understanding the drivers for circulation half-life: a polyethylene glycol versus 1,2-dipalmitoyl-sn-glycero-3-phosphodiglycerol study. J Control Release. 2021;333:1–15. doi:10.1016/j.jconrel.2021.03.014
  • Li L, Ten Hagen TL, Hossann M, et al. Mild hyperthermia triggered doxorubicin release from optimized stealth thermosensitive liposomes improves intratumoral drug delivery and efficacy. J Control Release. 2013;168(2):142–150. doi:10.1016/j.jconrel.2013.03.011
  • Lokerse WJM, Kneepkens ECM, Ten Hagen TLM, Eggermont AMM, Grüll H, Koning GA. In depth study on thermosensitive liposomes: optimizing formulations for tumor specific therapy and in vitro to in vivo relations. Biomaterials. 2016;82:138–150. doi:10.1016/j.biomaterials.2015.12.023
  • Miller CR, Bondurant B, McLean SD, McGovern KA, O’Brien DF. Liposome-cell interactions in vitro: effect of liposome surface charge on the binding and endocytosis of conventional and sterically stabilized liposomes. Biochemistry. 1998;37(5):12875–12883. doi:10.1021/bi980096y
  • Webb MS, Saxon D, Wong FM, et al. Comparison of different hydrophobic anchors conjugated to poly(ethylene glycol): effects on the pharmacokinetics of liposomal vincristine. Biochim Biophys Acta. 1998;1372(2):272–282. doi:10.1016/S0005-2736(98)00077-7
  • Majzoub RN, Chan CL, Ewert KK, et al. Uptake and transfection efficiency of PEGylated cationic liposome-DNA complexes with and without RGD-tagging. Biomaterials. 2014;35(18):4996–5005. doi:10.1016/j.biomaterials.2014.03.007
  • Kono Y, Iwasaki A, Fujita T. Effect of surface charge, particle size, and modification by polyethylene glycol of liposomes on their association with Caco-2 cells across an unstirred water layer. Pharmazie. 2018;73(1):3–8. doi:10.1691/ph.2018.7110
  • Kono Y, Jinzai H, Kotera Y, Fujita T. Influence of physicochemical properties and PEG modification of magnetic liposomes on their interaction with intestinal epithelial Caco-2 cells. Biol Pharm Bull. 2017;40(12):2166–2174. doi:10.1248/bpb.b17-00563
  • Song LY, Ahkong QF, Rong Q, et al. Characterization of the inhibitory effect of PEG-lipid conjugates on the intracellular delivery of plasmid and antisense DNA mediated by cationic lipid liposomes. Biochim Biophys Acta. 2002;1558(1):1–13. doi:10.1016/S0005-2736(01)00399-6
  • Lindner LH, Brock R, Arndt-Jovin D, Eibl H. Structural variation of cationic lipids: minimum requirement for improved oligonucleotide delivery into cells. J Control Release. 2006;110(2):444–456. doi:10.1016/j.jconrel.2005.10.009
  • Banerjee R, Mahidhar YV, Chaudhuri A, Gopal V, Rao NM. Design, synthesis, and transfection biology of novel cationic glycolipids for use in liposomal gene delivery. J Med Chem. 2001;44(24):4176–4185. doi:10.1021/jm000466s
  • Dicheva BM, Ten Hagen TL, Schipper D, et al. Targeted and heat-triggered doxorubicin delivery to tumors by dual targeted cationic thermosensitive liposomes. J Control Release. 2014;195:37–48. doi:10.1016/j.jconrel.2014.07.058
  • Lindner LH, Hossann M, Vogeser M, et al. Dual role of hexadecylphosphocholine (miltefosine) in thermosensitive liposomes: active ingredient and mediator of drug release. J Control Release. 2008;125(2):112–120. doi:10.1016/j.jconrel.2007.10.009
  • Overgaard J. Combined adriamycin and hyperthermia treatment of a murine mammary carcinoma in vivo. Cancer Res. 1976;36(9):3077–3081.
  • Chonn A, Cullis PR, Devine DV. The role of surface charge in the activation of the classical and alternative pathways of complement by liposomes. J Immunol. 1991;146(12):4234–4241.
  • Shan X, Yuan Y, Liu C, Tao X, Sheng Y, Xu F. Influence of PEG chain on the complement activation suppression and longevity in vivo prolongation of the PCL biomedical nanoparticles. Biomed Microdevices. 2009;11(6):1187–1194. doi:10.1007/s10544-009-9336-2
  • Zhao W, Zhuang S, Qi XR. Comparative study of the in vitro and in vivo characteristics of cationic and neutral liposomes. Int J Nanomedicine. 2011;6:3087–3098. doi:10.2147/IJN.S25399