Conveying a newly designed hydrophilic anti-human thymidylate synthase peptide to cisplatin resistant cancer cells: are pH-sensitive liposomes more effective than conventional ones?

References

• Estanqueiro M, Amaral MH, Conceição J, Sousa Lobo JM. Nanotechnological carriers for cancer chemotherapy: the state of the art. Colloids Surf B Biointerfaces 2015;126:631–48.
   PubMed Web of Science ®Google Scholar
• Krieger ML, Eckstein N, Schneider V, et al. Overcoming cisplatin resistance of ovarian cancer cells by targeted liposomes in vitro. Int J Pharm 2010;389:10–17.
   PubMed Web of Science ®Google Scholar
• Taddia L, D’Arca D, Ferrari S, et al. Inside the biochemical pathways of thymidylate synthase perturbed by anticancer drugs: novel strategies to overcome cancer chemoresistance. Drug Resist Updat 2015;23:20–54.
   PubMed Web of Science ®Google Scholar
• Colombo P-E, Fabbro M, Theillet C, et al. Sensitivity and resistance to treatment in the primary management of epithelial ovarian cancer. Crit Rev Oncol Hematol 2014;89:207–16.
   PubMed Web of Science ®Google Scholar
• Ferreira DDS, Lopes SC, de A, Franco MS, Oliveira MC. pH-sensitive liposomes for drug delivery in cancer treatment. Ther Deliv 2013;4:1099–123.
   PubMedGoogle Scholar
• Ricart AD, Berlin JD, Papadopoulos KP, et al. Phase I, pharmacokinetic and biological correlative study of OSI-7904L, a novel liposomal thymidylate synthase inhibitor, and cisplatin in patients with solid tumors. Clin Cancer Res 2008;14:7947–55.
   PubMed Web of Science ®Google Scholar
• Cardinale D, Guaitoli G, Tondi D, et al. Protein-protein interface-binding peptides inhibit the cancer therapy target human thymidylate synthase. Proc Natl Acad Sci USA 2011;108:E542–9.
   PubMed Web of Science ®Google Scholar
• Pelà M, Saxena P, Luciani R, et al. Optimization of peptides that target human thymidylate synthase to inhibit ovarian cancer cell growth. J Med Chem 2014;57:1355–67.
   PubMed Web of Science ®Google Scholar
• Hillaireau H, Couvreur P. Nanocarriers’ entry into the cell: relevance to drug delivery. Cell Mol Life Sci 2009;66:2873–96.
   PubMed Web of Science ®Google Scholar
• Sahay G, Alakhova DY, Kabanov AV. Endocytosis of nanomedicines. J Control Release 2010;145:182–95.
   PubMed Web of Science ®Google Scholar
• Collins D. pH-sensitive liposomes as tools for cytoplasmic delivery. In: Philippot JR, Schuber F, editors. Liposomes as tools in basic research and industry. Boca Raton, FL: CRC Press; 1995. pp. 201–214.
   Google Scholar
• Simões S, Moreira JN, Fonseca C, et al. On the formulation of pH-sensitive liposomes with long circulation times. Adv Drug Deliv Rev 2004;56:947–65.
   PubMed Web of Science ®Google Scholar
• Hafez IM, Cullis PR. Cholesteryl hemisuccinate exhibits pH sensitive polymorphic phase behavior. Biochim Biophys Acta 2000;1463:107–14.
   PubMed Web of Science ®Google Scholar
• Karanth H, Murthy RS. pH-sensitive liposomes-principle and application in cancer therapy. J Pharm Pharmacol 2007;59:469–83.
   PubMed Web of Science ®Google Scholar
• Simões S, Slepushkin V, Düzgünes N, Pedroso de Lima MC. On the mechanisms of internalization and intracellular delivery mediated by pH-sensitive liposomes. Biochim Biophys Acta 2001;1515:23–37.
   PubMed Web of Science ®Google Scholar
• Gregoriadis G, Davis C. Stability of liposomes in vivo and in vitro is promoted by their cholesterol content and the presence of blood cells. Biochem Biophys Res Commun 1979;89:1287–93.
   PubMed Web of Science ®Google Scholar
• Leite EA, Giuberti C, dos S, Wainstein AJ, et al. Acute toxicity of long-circulating and pH-sensitive liposomes containing cisplatin in mice after intraperitoneal administration. Life Sci 2009;84:641–9.
   PubMed Web of Science ®Google Scholar
• Cannazza G, Cazzato AS, Marraccini C, et al. Internalization and stability of a thymidylate synthase peptide inhibitor in ovarian cancer cells. J Med Chem 2014;57:10551–6.
   PubMed Web of Science ®Google Scholar
• Sacchetti F, Marraccini C, D’Arca D, et al. Enhanced anti-hyperproliferative activity of human thymidylate synthase inhibitor peptide by solid lipid nanoparticle delivery. Colloids Surf B Biointerfaces 2015;136:346–54.
   PubMed Web of Science ®Google Scholar
• DiSaia PJ, Sinkovics JG, Rutledge FN, Smith JP. Cell-mediated immunity to human malignant cells. A brief review and further studies with two gynecologic tumors. Am J Obstet Gynecol 1972;114:979–89.
   PubMed Web of Science ®Google Scholar
• Andrews PA, Murphy MP, Howell SB. Differential potentiation of alkylating and platinating agent cytotoxicity in human ovarian carcinoma cells by glutathione depletion. Cancer Res 1985;45:6250–3.
   PubMed Web of Science ®Google Scholar
• Giuberti CS, Boratto FA, Degobert G, et al. Investigation of alternative organic solvents and methods for the preparation of long-circulating and pH-sensitive liposomes containing cisplatin. J Liposome Res 2013;23:220–7.
   PubMed Web of Science ®Google Scholar
• Pidgeon C, McNeely S, Schmidt T, Johnson JE. Multilayered vesicles prepared by reverse-phase evaporation: liposome structure and optimum solute entrapment. Biochemistry 1987;26:17–29.
   PubMed Web of Science ®Google Scholar
• Szoka F, Papahadjopoulos D. Procedure for preparation of liposomes with large internal aqueous space and high capture by reverse-phase evaporation. Proc Natl Acad Sci USA 1978;75:4194–8.
   PubMed Web of Science ®Google Scholar
• Murdock RC, Braydich-Stolle L, Schrand AM, et al. Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicol Sci 2008;101:239–53.
   PubMed Web of Science ®Google Scholar
• Chang M, Lu S, Zhang F, et al. RGD-modified pH-sensitive liposomes for docetaxel tumor targeting. Colloids Surf B Biointerfaces 2015;129:175–82.
   PubMed Web of Science ®Google Scholar
• Drummond DC, Zignani M, Leroux J. C. Current status of pH-sensitive liposomes in drug delivery. Prog Lipid Res 2000;39:409–60.
   PubMed Web of Science ®Google Scholar
• Van den Bossche J, Al-Jamal WT, Yilmazer A, et al. Intracellular trafficking and gene expression of pH-sensitive, artificially enveloped adenoviruses in vitro and in vivo. Biomaterials 2011;32:3085–93.
   PubMed Web of Science ®Google Scholar
• Oumzil K, Benizri S, Tonelli G, et al. pH-cleavable nucleoside lipids: a new paradigm for controlling the stability of lipid-based delivery systems. ChemMedChem 2015;10:1797–801.
   PubMed Web of Science ®Google Scholar
• Ron-Doitch S, Sawodny B, Kühbacher A, et al. Reduced cytotoxicity and enhanced bioactivity of cationic antimicrobial peptides liposomes in cell cultures and 3D epidermis model against HSV. J Control Release 2016;229:163–71.
   PubMed Web of Science ®Google Scholar
• Mohan A, Rajendran SRCK, He QS, et al. Encapsulation of food protein hydrolysates and peptides: a review. RSC Adv 2015;5:79270–8.
   Web of Science ®Google Scholar
• Swaminathan J, Ehrhardt C. Liposomal delivery of proteins and peptides. Expert Opin Drug Deliv 2012;9:1489–503.
   PubMed Web of Science ®Google Scholar
• Martins S, Sarmento B, Ferreira DC, Souto EB. Lipid-based colloidal carriers for peptide and protein delivery–liposomes versus lipid nanoparticles. Int J Nanomedicine 2007;2:595–607.
   PubMed Web of Science ®Google Scholar
• Xie Y, Ye L, Zhang X, et al. Transport of nerve growth factor encapsulated into liposomes across the blood-brain barrier: in vitro and in vivo studies. J Control Release 2005;105:106–19.
   PubMed Web of Science ®Google Scholar
• Chen W, Huang L. Induction of cytotoxic T-lymphocytes and antitumor activity by a liposomal lipopeptide vaccine. Mol Pharm 2008;5:464–71.
   PubMed Web of Science ®Google Scholar
• Tandrup Schmidt S, Foged C, Korsholm KS, et al. Liposome-based adjuvants for subunit vaccines: formulation strategies for subunit antigens and immunostimulators. Pharmaceutics 2016;8:7–29.
   PubMed Web of Science ®Google Scholar
• Ramachandran S, Quist AP, Kumar S, Lal R. Cisplatin nanoliposomes for cancer therapy: AFM and fluorescence imaging of cisplatin encapsulation, stability, cellular pptake, and toxicity. Langmuir 2006;22:8156–62.
   PubMed Web of Science ®Google Scholar
• Chu CJ, Dijkstra J, Lai MZ, et al. Efficiency of cytoplasmic delivery by pH-sensitive liposomes to cells in culture. Pharm Res 1990;7:824–34.
   PubMed Web of Science ®Google Scholar
• Ghanbarzadeh S, Khorrami A, Mohamed Khosroshahi L, Arami S. Fusogenic pH sensitive liposomal formulation for rapamycin: improvement of antiproliferative effect. Pharm Biol 2014;52:848–54.
   PubMed Web of Science ®Google Scholar
• Stewart MP, Lorenz A, Dahlman J, Sahay G. Challenges in carrier-mediated intracellular delivery: moving beyond endosomal barriers. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2016;8:465–78.
   PubMed Web of Science ®Google Scholar
• Deng ZJ, Morton SW, Bonner DK, et al. A plug-and-play ratiometric pH-sensing nanoprobe for high-throughput investigation of endosomal escape. Biomaterials 2015;51:250–6.
   PubMed Web of Science ®Google Scholar