Effects of PEG-Linker Chain Length of Folate-Linked Liposomal Formulations on Targeting Ability and Antitumor Activity of Encapsulated Drug

References

• Atlihan-Gundogdu E, Ilem-Ozdemir D, Ekinci M, et al. Recent developments in cancer therapy and diagnosis. J Pharm Investig. 2020;50:1–13.
   Web of Science ®Google Scholar
• Tran P, Lee S-E, Kim D-H, Pyo Y-C, Park J-SJ. Recent advances of nanotechnology for the delivery of anticancer drugs for breast cancer treatment. J Pharm Investig. 2020;50(3):261–270.
   Web of Science ®Google Scholar
• Gupta B, Kim JOJ. Recent progress in cancer immunotherapy approaches based on nanoparticle delivery devices. J Pharm Investig. 2021;51:1–14.
   Web of Science ®Google Scholar
• Ha E-S, Kang H-T, Park H, Kim S, Kim M-S. Advanced technology using supercritical fluid for particle production in pharmaceutical continuous manufacturing. J Pharm Investig. 2022;2022. doi:10.1007/s40005-022-00601-y
   Google Scholar
• Doane TL, Burda C. The unique role of nanoparticles in nanomedicine: imaging, drug delivery and therapy. Chem Soc Rev. 2012;41(7):2885–2911. doi:10.1039/C2CS15260F
   PubMed Web of Science ®Google Scholar
• Wagner V, Dullaart A, Bock A-K, Zweck A. The emerging nanomedicine landscape. Nat Biotechnol. 2006;24(10):1211–1217. doi:10.1038/nbt1006-1211
   PubMed Web of Science ®Google Scholar
• Kiio TM, Park SJ. Physical properties of nanoparticles do matter. J Pharm Investig. 2021;51(1):35–51.
   Web of Science ®Google Scholar
• Hoang NH, Lim C, Sim T, Oh KT. Triblock copolymers for nano-sized drug delivery systems. J Pharm Investig. 2017;47(1):27–35. doi:10.1007/s40005-016-0291-7
   Google Scholar
• Son G-H, Lee B-J, Cho C-W. Mechanisms of drug release from advanced drug formulations such as polymeric-based drug-delivery systems and lipid nanoparticles. J Pharm Investig. 2017;47(4):287–296. doi:10.1007/s40005-017-0320-1
   Google Scholar
• Uhrich KE, Cannizzaro SM, Langer RS, Shakesheff KM. Polymeric systems for controlled drug release. Chem Rev. 1999;99(11):3181–3198. doi:10.1021/cr940351u
   PubMed Web of Science ®Google Scholar
• Cho H-J. Recent progresses in the development of hyaluronic acid-based nanosystems for tumor-targeted drug delivery and cancer imaging. J Pharm Investig. 2020;50(2):115–129.
   Web of Science ®Google Scholar
• Shinn J, Kwon N, Lee SA, Lee Y. Smart pH-responsive nanomedicines for disease therapy. J Pharm Investig. 2022;52(4):427–441. doi:10.1007/s40005-022-00573-z
   PubMed Web of Science ®Google Scholar
• Hua S, Wu S. The use of lipid-based nanocarriers for targeted pain therapies. Mini Review. Front Pharmacol. 2013;4(143). doi:10.3389/fphar.2013.00143
   Google Scholar
• Lim C, Kang JK, Won WR, et al. Co-delivery of D-(KLAKLAK)2 peptide and chlorin e6 using a liposomal complex for synergistic cancer therapy. Pharmaceutics. 2019;11(6):293. doi:10.3390/pharmaceutics11060293
   PubMed Web of Science ®Google Scholar
• Nogueira E, Gomes AC, Preto A, Cavaco-Paulo A. Design of liposomal formulations for cell targeting. Colloids Surf B Biointerfaces. 2015;136:514–526. doi:10.1016/j.colsurfb.2015.09.034
   PubMed Web of Science ®Google Scholar
• Patil Y, Amitay Y, Ohana P, Shmeeda H, Gabizon A. Targeting of pegylated liposomal mitomycin-C prodrug to the folate receptor of cancer cells: intracellular activation and enhanced cytotoxicity. J Control Release. 2016;225:87–95. doi:10.1016/j.jconrel.2016.01.039
   PubMed Web of Science ®Google Scholar
• Sadzuka Y, Sugiyama I, Tsuruda T, Sonobe T. Characterization and cytotoxicity of mixed polyethyleneglycol modified liposomes containing doxorubicin. Int J Pharm. 2006;312(1):83–89. doi:10.1016/j.ijpharm.2005.12.043
   PubMedGoogle Scholar
• Hegde MM, Prabhu S, Mutalik S, Chatterjee A, Goda JS, Satish Rao BS. Multifunctional lipidic nanocarriers for effective therapy of glioblastoma: recent advances in stimuli-responsive, receptor and subcellular targeted approaches. J Pharm Investig. 2022;52(1):49–74. doi:10.1007/s40005-021-00548-6
   Web of Science ®Google Scholar
• Gabizon A, Shmeeda H, Barenholz Y. Pharmacokinetics of pegylated liposomal doxorubicin. Clin Pharmacokinet. 2003;42(5):419–436. doi:10.2165/00003088-200342050-00002
   PubMed Web of Science ®Google Scholar
• Hamidi M, Azadi A, Rafiei P. Pharmacokinetic Consequences of Pegylation. Drug Deliv. 2006;13(6):399–409. doi:10.1080/10717540600814402
   PubMed Web of Science ®Google Scholar
• Muthu MS, Kulkarni SA, 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. doi:10.1016/j.ijpharm.2011.09.045
   PubMed Web of Science ®Google Scholar
• Singh S. Liposome encapsulation of doxorubicin and celecoxib in combination inhibits progression of human skin cancer cells. Int J Nanomedicine. 2018;13:11–13. doi:10.2147/IJN.S124701
   PubMedGoogle Scholar
• Noble GT, Stefanick JF, Ashley JD, Kiziltepe T, Bilgicer B. Ligand-targeted liposome design: challenges and fundamental considerations. Trends Biotechnol. 2014;32(1):32–45. doi:10.1016/j.tibtech.2013.09.007
   PubMed Web of Science ®Google Scholar
• Suzuki R, Takizawa T, Kuwata Y, et al. Effective anti-tumor activity of oxaliplatin encapsulated in transferrin–PEG-liposome. Int J Pharm. 2008;346(1):143–150. doi:10.1016/j.ijpharm.2007.06.010
   PubMedGoogle Scholar
• Zhang N, Li C, Zhou D, et al. Cyclic RGD functionalized liposomes encapsulating urokinase for thrombolysis. Acta Biomaterialia. 2018;70:227–236. doi:10.1016/j.actbio.2018.01.038
   PubMed Web of Science ®Google Scholar
• Nie S. Understanding and overcoming major barriers in cancer nanomedicine. Nanomedicine. 2010;5(4):523–528. doi:10.2217/nnm.10.23
   PubMed Web of Science ®Google Scholar
• Biswas S, Deshpande PP, Perche F, Dodwadkar NS, Sane SD, Torchilin VP. Octa-arginine-modified pegylated liposomal doxorubicin: an effective treatment strategy for non-small cell lung cancer. Cancer Lett. 2013;335(1):191–200. doi:10.1016/j.canlet.2013.02.020
   PubMed Web of Science ®Google Scholar
• Jiang T, Zhang Z, Zhang Y, et al. Dual-functional liposomes based on pH-responsive cell-penetrating peptide and hyaluronic acid for tumor-targeted anticancer drug delivery. Biomaterials. 2012;33(36):9246–9258. doi:10.1016/j.biomaterials.2012.09.027
   PubMed Web of Science ®Google Scholar
• Moret F, Scheglmann D, Reddi E. Folate-targeted PEGylated liposomes improve the selectivity of PDT with meta-tetra(hydroxyphenyl)chlorin (m-THPC). Photochem Photobiol Sci. 2013;12(5):823–834. doi:10.1039/C3PP25384H
   PubMed Web of Science ®Google Scholar
• Sun M, Wang Y, Shen J, Xiao Y, Su Z, Ping Q. Octreotide-modification enhances the delivery and targeting of doxorubicin-loaded liposomes to somatostatin receptors expressing tumor in vitro and in vivo. Nanotechnology. 2010;21(47):475101. doi:10.1088/0957-4484/21/47/475101
   PubMed Web of Science ®Google Scholar
• Sahu BP, Baishya R, Hatiboruah JL, Laloo D, Biswas N. A comprehensive review on different approaches for tumor targeting using nanocarriers and recent developments with special focus on multifunctional approaches. J Pharm Investig. 2022;52(5):539–585. doi:10.1007/s40005-022-00583-x
   Web of Science ®Google Scholar
• LeBeau AM, Duriseti S, Murphy ST, et al. Targeting uPAR with antagonistic recombinant human antibodies in aggressive breast cancer. Cancer Res. 2013;73(7):2070. doi:10.1158/0008-5472.CAN-12-3526
   PubMed Web of Science ®Google Scholar
• Wu J, Liu Q, Lee RJ. A folate receptor-targeted liposomal formulation for paclitaxel. Int J Pharm. 2006;316(1):148–153. doi:10.1016/j.ijpharm.2006.02.027
   PubMedGoogle Scholar
• Shim G, Jeong S, Oh JL, Kang Y. Lipid-based nanoparticles for photosensitive drug delivery systems. J Pharm Investig. 2022;52(2):151–160. doi:10.1007/s40005-021-00553-9
   PubMed Web of Science ®Google Scholar
• Farokhzad OC, Langer R. Impact of nanotechnology on drug delivery. ACS Nano. 2009;3(1):16–20. doi:10.1021/nn900002m
   PubMed Web of Science ®Google Scholar
• Ferrari M. Cancer nanotechnology: opportunities and challenges. Nat Rev Cancer. 2005;5(3):161–171. doi:10.1038/nrc1566
   PubMed Web of Science ®Google Scholar
• Gabizon A, Horowitz AT, Goren D, Tzemach D, Shmeeda H, Zalipsky S. In vivo fate of folate-targeted polyethylene-glycol liposomes in tumor-bearing mice. Clin Cancer Res. 2003;9(17):6551.
   PubMed Web of Science ®Google Scholar
• Saw PE, Park J, Lee E, et al. Effect of PEG pairing on the efficiency of cancer-targeting liposomes. Theranostics. 2015;5(7):746–754. doi:10.7150/thno.10732
   PubMed Web of Science ®Google Scholar
• Stefanick JF, Ashley JD, Kiziltepe T, Bilgicer B. A systematic analysis of peptide linker length and liposomal polyethylene glycol coating on cellular uptake of peptide-targeted liposomes. ACS Nano. 2013;7(4):2935–2947. doi:10.1021/nn305663e
   PubMed Web of Science ®Google Scholar
• Kirpotin D, Park JW, Hong K, et al. Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry. 1997;36(1):66–75. doi:10.1021/bi962148u
   PubMed Web of Science ®Google Scholar
• Sapra P, Tyagi P, Allen TM. Ligand-targeted liposomes for cancer treatment. Curr Drug Deliv. 2005;2(4):369–381. doi:10.2174/156720105774370159
   PubMedGoogle Scholar
• Yamada A, Taniguchi Y, Kawano K, Honda T, Hattori Y, Maitani Y. Design of folate-linked liposomal doxorubicin to its antitumor effect in mice. Clin Cancer Res. 2008;14(24):8161. doi:10.1158/1078-0432.CCR-08-0159
   PubMed Web of Science ®Google Scholar
• Bakhtiar A, Liew QX, Ng KY, Chowdhury EH. Active targeting via ligand-anchored pH-responsive strontium nanoparticles for efficient nucleic acid delivery into breast cancer cells. J Pharm Investig. 2022;52(2):243–257. doi:10.1007/s40005-022-00559-x
   Web of Science ®Google Scholar
• Lu Y, Low PS. Folate-mediated delivery of macromolecular anticancer therapeutic agents. Adv Drug Deliv Rev. 2012;64:342–352. doi:10.1016/j.addr.2012.09.020
   Web of Science ®Google Scholar
• Marshalek JP, Sheeran PS, Ingram P, Dayton PA, Witte RS, Matsunaga TO. Intracellular delivery and ultrasonic activation of folate receptor-targeted phase-change contrast agents in breast cancer cells in vitro. J Control Release. 2016;243:69–77. doi:10.1016/j.jconrel.2016.09.010
   PubMed Web of Science ®Google Scholar
• Muralidharan R, Babu A, Amreddy N, et al. Folate receptor-targeted nanoparticle delivery of HuR-RNAi suppresses lung cancer cell proliferation and migration. J Nanobiotechnology. 2016;14(1):47. doi:10.1186/s12951-016-0201-1
   PubMed Web of Science ®Google Scholar
• Siwowska K, Schmid RM, Cohrs S, Schibli R, Müller C. Folate receptor-positive gynecological cancer cells: in vitro and in vivo characterization. Pharmaceuticals. 2017;10(3):72. doi:10.3390/ph10030072
   Web of Science ®Google Scholar
• Mirzaghavami PS, Khoei S, Khoee S, Shirvalilou S. Folic acid-conjugated magnetic triblock copolymer nanoparticles for dual targeted delivery of 5-fluorouracil to colon cancer cells. Cancer Nanotechnol. 2022;13(1):12. doi:10.1186/s12645-022-00120-3
   Web of Science ®Google Scholar
• Chango A, Emery-Fillon N, de Courcy GP, et al. A polymorphism (80G->A) in the reduced folate carrier gene and its associations with folate status and homocysteinemia. Mol Genet Metab. 2000;70(4):310–315. doi:10.1006/mgme.2000.3034
   PubMed Web of Science ®Google Scholar
• Wang S, Low PS. Folate-mediated targeting of antineoplastic drugs, imaging agents, and nucleic acids to cancer cells. J Control Release. 1998;53(1):39–48. doi:10.1016/S0168-3659(97)00236-8
   PubMed Web of Science ®Google Scholar
• Chen Y, Minh LV, Liu J, et al. Baicalin loaded in folate-PEG modified liposomes for enhanced stability and tumor targeting. Colloids Surf B Biointerfaces. 2016;140:74–82. doi:10.1016/j.colsurfb.2015.11.018
   PubMed Web of Science ®Google Scholar
• Nho TDT, Ly HT, Vo TS, et al. Enhanced anticancer efficacy and tumor targeting through folate-PEG modified nanoliposome loaded with 5-fluorouracil. Adv Nat Sci Nanosci Nanotechnol. 2017;8(1):015008.
   Google Scholar
• Gabizon A, Horowitz AT, Goren D, et al. Targeting folate receptor with folate linked to extremities of poly(ethylene glycol)-grafted liposomes: in vitro studies. Bioconjug Chem. 1999;10(2):289–298. doi:10.1021/bc9801124
   PubMed Web of Science ®Google Scholar
• Kawano K, Maitani Y. Effects of polyethylene glycol spacer length and ligand density on folate receptor targeting of liposomal Doxorubicin in vitro. J Drug Deliv. 2011;2011:1–6. doi:10.1155/2011/160967
   Google Scholar
• Riviere K, Huang Z, Jerger K, Macaraeg N, Szoka FC. Antitumor effect of folate-targeted liposomal doxorubicin in KB tumor-bearing mice after intravenous administration. J Drug Target. 2011;19(1):14–24. doi:10.3109/10611861003733953
   PubMed Web of Science ®Google Scholar
• Gabizon A, Shmeeda H, Horowitz AT, Zalipsky S. Tumor cell targeting of liposome-entrapped drugs with phospholipid-anchored folic acid–PEG conjugates. Adv Drug Deliv Rev. 2004;56(8):1177–1192. doi:10.1016/j.addr.2004.01.011
   PubMed Web of Science ®Google Scholar
• Qu M-H, Zeng R-F, Fang S, Dai Q-S, Li H-P, Long J-T. Liposome-based co-delivery of siRNA and docetaxel for the synergistic treatment of lung cancer. Int J Pharm. 2014;474(1):112–122. doi:10.1016/j.ijpharm.2014.08.019
   PubMedGoogle Scholar
• Park JY, Shin Y, Won WR, et al. Development of AE147 peptide-conjugated nanocarriers for targeting uPAR-overexpressing cancer cells. Int J Nanomedicine. 2021;16:5437. doi:10.2147/IJN.S315619
   PubMed Web of Science ®Google Scholar
• Zucker D, Marcus D, Barenholz Y, Goldblum A. Liposome drugs’ loading efficiency: a working model based on loading conditions and drug’s physicochemical properties. J Control Release. 2009;139(1):73–80. doi:10.1016/j.jconrel.2009.05.036
   PubMed Web of Science ®Google Scholar
• Yuan M, Qiu Y, Zhang L, Gao H, He Q. Targeted delivery of transferrin and TAT co-modified liposomes encapsulating both paclitaxel and doxorubicin for melanoma. Drug Deliv. 2016;23(4):1171–1183. doi:10.3109/10717544.2015.1040527
   PubMed Web of Science ®Google Scholar
• Park EJ, Jun HW, Na IH, et al. CD48-expressing non-small-cell lung cancer cells are susceptible to natural killer cell–mediated cytotoxicity. Arch Pharm Res. 2022;45(1):1–10. doi:10.1007/s12272-021-01365-z
   PubMed Web of Science ®Google Scholar
• Hwang D, Dismuke T, Tikunov A, et al. Poly(2-oxazoline) nanoparticle delivery enhances the therapeutic potential of vismodegib for medulloblastoma by improving CNS pharmacokinetics and reducing systemic toxicity. Nanomedicine. 2021;32:102345. doi:10.1016/j.nano.2020.102345
   PubMed Web of Science ®Google Scholar
• Epps DE, Raub TJ, Caiolfa V, Chiari A, Zamai M. Determination of the affinity of drugs toward serum albumin by measurement of the quenching of the intrinsic tryptophan fluorescence of the protein. J Pharm Pharmacol. 1999;51(1):41–48. doi:10.1211/0022357991772079
   PubMed Web of Science ®Google Scholar
• Wang F, Yu R, Wen S, et al. Overexpressing microRNA-203 alleviates myocardial infarction via interacting with long non-coding RNA MIAT and mitochondrial coupling factor 6. Arch Pharm Res. 2021;44(5):525–535. doi:10.1007/s12272-021-01324-8
   PubMed Web of Science ®Google Scholar
• Nam S, Na HG, Oh EH, et al. Discovery and synthesis of 1,2,4-oxadiazole derivatives as novel inhibitors of Zika, dengue, Japanese encephalitis, and classical swine fever virus infections. Arch Pharm Res. 2022;45(4):280–293. doi:10.1007/s12272-022-01380-8
   PubMed Web of Science ®Google Scholar
• Lee S, Pham D-V, Park P-H. Sestrin2 induction contributes to anti-inflammatory responses and cell survival by globular adiponectin in macrophages. Arch Pharm Res. 2022;45(1):38–50. doi:10.1007/s12272-021-01364-0
   PubMed Web of Science ®Google Scholar
• Dos Santos N, Allen C, Doppen A-M, et al. Influence of poly(ethylene glycol) grafting density and polymer length on liposomes: relating plasma circulation lifetimes to protein binding. Biochimica et Biophysica Acta. 2007;1768(6):1367–1377. doi:10.1016/j.bbamem.2006.12.013
   PubMed Web of Science ®Google Scholar
• Bulbake U, Doppalapudi S, Kommineni N, Khan W. Liposomal formulations in clinical use: an updated review. Pharmaceutics. 2017;9(2):12. doi:10.3390/pharmaceutics9020012
   PubMed Web of Science ®Google Scholar
• Hattori Y, Maitani Y. Enhanced in vitro DNA transfection efficiency by novel folate-linked nanoparticles in human prostate cancer and oral cancer. J Control Release. 2004;97(1):173–183. doi:10.1016/j.jconrel.2004.03.007
   PubMed Web of Science ®Google Scholar
• Ohguchi Y, Kawano K, Hattori Y, Maitani Y. Selective delivery of folate–PEG-linked, nanoemulsion-loaded aclacinomycin A to KB nasopharyngeal cells and xenograft: effect of chain length and amount of folate–PEG linker. J Drug Target. 2008;16(9):660–667. doi:10.1080/10611860802201464
   PubMed Web of Science ®Google Scholar
• Shiokawa T, Hattori Y, Kawano K, et al. Effect of polyethylene glycol linker chain length of folate-linked microemulsions loading aclacinomycin a on targeting ability and antitumor effect in vitro and in vivo. Clin Cancer Res. 2005;11(5):2018. doi:10.1158/1078-0432.CCR-04-1129
   PubMed Web of Science ®Google Scholar
• Hinrichs WLJ, Manceñido FA, Sanders NN, et al. The choice of a suitable oligosaccharide to prevent aggregation of PEGylated nanoparticles during freeze thawing and freeze drying. Int J Pharm. 2006;311(1):237–244. doi:10.1016/j.ijpharm.2005.12.032
   PubMedGoogle Scholar
• Xiang G, Wu J, Lu Y, Liu Z, Lee RJ. Synthesis and evaluation of a novel ligand for folate-mediated targeting liposomes. Int J Pharm. 2008;356(1):29–36. doi:10.1016/j.ijpharm.2007.12.030
   PubMedGoogle Scholar
• Fang C, Shi B, Pei Y-Y. Effect of MePEG molecular weight and particle size on in vitro release of tumor necrosis factor-α-loaded nanoparticles. Acta Pharmacol Sin. 2005;26(2):242–249. doi:10.1111/j.1745-7254.2005.00537.x
   PubMed Web of Science ®Google Scholar
• Kim J-Y, Kim J-K, Park J-S, Byun Y, Kim C-K. The use of PEGylated liposomes to prolong circulation lifetimes of tissue plasminogen activator. Biomaterials. 2009;30(29):5751–5756. doi:10.1016/j.biomaterials.2009.07.021
   PubMed Web of Science ®Google Scholar
• Shmeeda H, Mak L, Tzemach D, Astrahan P, Tarshish M, Gabizon A. Intracellular uptake and intracavitary targeting of folate-conjugated liposomes in a mouse lymphoma model with up-regulated folate receptors. Mol Cancer Ther. 2006;5(4):818–824. doi:10.1158/1535-7163.MCT-05-0543
   PubMed Web of Science ®Google Scholar
• Wang F, Xiao W, Elbahnasawy MA, et al. Optimization of the linker length of mannose-cholesterol conjugates for enhanced mRNA delivery to dendritic cells by liposomes. Front Pharmacol. 2018;9:980. doi:10.3389/fphar.2018.00980
   PubMed Web of Science ®Google Scholar
• Xing H, Li J, Xu W, et al. The effects of spacer length and composition on aptamer-mediated cell-specific targeting with nanoscale PEGylated liposomal doxorubicin. Chembiochem. 2016;17(12):1111–1117. doi:10.1002/cbic.201600092
   PubMed Web of Science ®Google Scholar
• Cavalli S, Tipton AR, Overhand M, Kros A. The chemical modification of liposome surfaces via a copper-mediated [3 + 2] azide–alkyne cycloaddition monitored by a colorimetric assay. Chem Comm. 2006;(30):3193–3195. doi:10.1039/B606930D
   PubMed Web of Science ®Google Scholar
• Kumar A, Erasquin UJ, Qin G, Li K, Cai C. “Clickable”, polymerized liposomes as a versatile and stable platform for rapid optimization of their peripheral compositions. Chem Comm. 2010;46(31):5746–5748. doi:10.1039/C0CC00784F
   PubMed Web of Science ®Google Scholar
• Feldborg LN, Jølck RI, Andresen TL. Quantitative evaluation of bioorthogonal chemistries for surface functionalization of nanoparticles. Bioconjug Chem. 2012;23(12):2444–2450. doi:10.1021/bc3005057
   PubMed Web of Science ®Google Scholar
• Kang MH, Yoo HJ, Kwon YH, et al. Design of multifunctional liposomal nanocarriers for folate receptor-specific intracellular drug delivery. Mol Pharm. 2015;12(12):4200–4213. doi:10.1021/acs.molpharmaceut.5b00399
   PubMed Web of Science ®Google Scholar