Lipopeptide-modified PEG-PE-based pharmaceutical nanocarriers for enhanced uptake in blood-brain barrier cells and improved cytotoxicity against glioma cells

European Journal of Lipid Science and Technology

Volumn 116, Issue 9, 2014, Pages 1174-1183

  Sydow, Karl ^a   Torchilin, Vladimir P ^b   Dathe, Margitta ^a  

^a LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Brain; Drug delivery; Glioma; Lipopeptide; Micelles; Nanoparticles

Indexed keywords

EID: 84912091589     PISSN: 14387697     EISSN: 14389312     Source Type: Journal    
DOI: 10.1002/ejlt.201300373     Document Type: Article

References (45)

1. Ohgaki, H., Kleihues, P., Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J. Neuropathol. Exp. Neurol. 2005, 64, 479.
2. Begley, D. J., Delivery of therapeutic agents to the central nervous system: The problems and the possibilities. Pharmacol. Ther. 2004, 104, 29-45.
3. Wolburg, H., Noell, S., Fallier-Becker, P., Mack, A. F., Wolburg-Buchholz, K., The disturbed blood-brain barrier in human glioblastoma. Mol. Aspects Med. 2012, 33, 579-589.
4. Yuhas, J. M., Li, A. P., Martinez, A. O., Ladman, A. J., A simplified method for production and growth of multicellular tumor spheroids. Cancer Res. 1977, 37, 3639-3643.
5. Zhai, M., Liang, C., Li, A., Chang, J. et al., Magnetic paclitaxel nanoparticles inhibit glioma growth and improve the survival of rats bearing glioma xenografts. Anticancer Res. 2010, 30, 2217-2223.
6. Zhang, P., Hu, L., Yin, Q., Feng, L., Li, Y., Transferrinmodified c[RGDfK]-paclitaxel loaded hybrid micelle for sequential blood-brain barrier penetration and glioma targeting therapy. Mol. Pharm. 2012, 9, 1590-1598.
7. Leupold, E., Nikolenko, H., Dathe, M., Apolipoprotein E peptide-modified colloidal carriers: The design determines the mechanism of uptake in vascular endothelial cells. BBA-Biomembranes 2009, 1788, 442-449.
8. Dyer, C. A. C., Curtiss, L. K. L., A synthetic peptide mimic of plasma apolipoprotein E that binds the LDL receptor. J. Biol. Chem. 1991, 266, 22803-22806.
9. Dehouck, B., Dehouck, M. P., Fruchart, J. C., Cecchelli, R., Upregulation of the low density lipoprotein receptor at the blood-brain barrier: Intercommunications between brain capillary endothelial cells and astrocytes. J. Cell Biol. 1994, 126, 465-473.
10. Maletínská, L., Blakely, E. A., Bjornstad, K. A., Deen, D. F. et al., Human glioblastoma cell lines: Levels of low-density lipoprotein receptor and low-density lipoprotein receptorrelated protein. Cancer Res. 2000, 60, 2300-2303.
11. Gehne, S., Sydow, K., Dathe, M., Kumke, M. U., Characterization of cell-penetrating lipopeptide micelles by spectroscopic methods. J. Phys. Chem. B 2013, 117, 14215-14225.
12. Wiley, D. T., Webster, P., Gale, A., Davis, M. E., Transcytosis and brain uptake of transferrin-containing nanoparticles by tuning avidity to transferrin receptor. PNAS 2013, 110, 8662-8667.
13. Richard, J. P., Melikov, K., Brooks, H., Prevot, P. et al., Cellular uptake of unconjugated TAT peptide involves clathrin-dependent endocytosis and heparan sulfate receptors. J. Biol. Chem. 2005, 280, 15300-15306.
14. Abouzeid, A. H., Patel, N. R., Rachman, I. M., Senn, S., Torchilin, V. P., Anti-cancer activity of anti-GLUT1 antibody-targeted polymeric micelles co-loaded with curcumin and doxorubicin. J. Drug. Target 2013, 21, 994-1000.
15. Salzano, G., Riehle, R., Navarro, G., Perche, F. et al., Polymeric micelles containing reversibly phospholipidmodified anti-survivin siRNA: A promising strategy to overcome drug resistance in cancer. Cancer Lett. 2014, 343, 224-231.
16. Twelves, C., Chmielowska, E., Havel, L., Popat, S. et al., Randomised phase II study of axitinib or bevacizumab combined with paclitaxel/carboplatin as first-line therapy for patients with advanced non-small-cell lung cancer. Ann. Oncol. 2014, 25, 132-138.
17. Baselga, J., Manikhas, A., Cortés, J., Llombart, A. et al., Phase III trial of nonpegylated liposomal doxorubicin in combination with trastuzumab and paclitaxel in HER2-positive metastatic breast cancer. Ann. Oncol. 2014, 25, 592-598.
18. Torchilin, V. P., Micellar nanocarriers: Pharmaceutical perspectives. Pharm. Res. 2007, 24, 1-16.
19. Ricci-Vitiani, L., Pallini, R., Biffoni, M., Todaro, M. et al., Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 2010, 468, 824-828.
20. Tseng, S. H., Bobola, M. S., Berger, M. S., Silber, J. R., Characterization of paclitaxel (Taxol1) sensitivity in human glioma-and medulloblastoma-derived cell lines. Neuro-Oncol. 1999, 1, 101-108.
21. Sauer, I., Dunay, I. R., Weisgraber, K., Bienert, M., Dathe, M., An apolipoprotein E-derived peptide mediates uptake of sterically stabilized liposomes into brain capillary endothelial cells. Biochemistry 2005, 44, 2021-2029.
22. Leupold, E., Nikolenko, H., Beyermann, M., Dathe, M., Insight into the role of HSPG in the cellular uptake of apolipoprotein E-derived peptide micelles and liposomes. Biochim. Biophys. Acta 2008, 1778, 2781-2789.
23. Lukyanov, A. N., Gao, Z., Torchilin, V. P., Micelles from polyethylene glycol/phosphatidylethanolamine conjugates for tumor drug delivery. J. Control. Release 2003, 91, 97-102.
24. Dabholkar, R. D., Sawant, R. M., Mongayt, D. A., Devarajan, P. V., Torchilin, V. P., Polyethylene glycol-phosphatidylethanolamine conjugate (PEG-PE)-based mixed micelles: Some properties, loading with paclitaxel, and modulation of P-glycoprotein-mediated efflux. Int. J. Pharm. 2006, 315, 148-157.
25. Wang, J., Mongayt, D., Torchilin, V. P., Polymeric micelles for delivery of poorly soluble drugs: Preparation and anticancer activity in vitro of paclitaxel incorporated into mixed micelles based on poly(ethylene glycol)-lipid conjugate and positively charged lipids. J. Drug. Target 2005, 13, 73-80.
26. Biswas, S., Deshpande, P. P., Perche, F., Dodwadkar, N. S. et al., Octa-arginine-modified pegylated liposomal doxorubicin: an effective treatment strategy for non-small cell lung cancer. Cancer Lett. 2013, 335, 191-200.
27. Keller, S., Sauer, I., Strauss, H., Gast, K. et al., Membranemimetic nanocarriers formed by a dipalmitoylated cellpenetrating peptide. Angew. Chem. Int. Ed. Engl. 2005, 44, 5252-5255.
28. Vucic, E., Sanders, H. M. H. F., Arena, F., Terreno, E. et al., Well-defined, multifunctional nanostructures of a paramagnetic lipid and a lipopeptide for macrophage imaging. J. Am. Chem. Soc. 2009, 131, 406-407.
29. Chen, J.-X., Wang, H.-Y., Quan, C.-Y., Xu, X.-D. et al., Amphiphilic cationic lipopeptides with RGD sequences as gene vectors. Org. Biomol. Chem. 2010, 8, 3142.
30. Fan, H. Y., Nazari, M., Raval, G., Khan, Z. et al., Utilizing zeta potential measurements to study the effective charge, membrane partitioning, and membrane permeation of the lipopeptide surfactin. BBA-Biomembranes 2014, 1-7.
31. Sawant, R. M., Hurley, J. P., Salmaso, S., Kale, A. et al., "SMART" drug delivery systems: Double-targeted pH-responsive pharmaceutical nanocarriers. Bioconjug. Chem. 2006, 17, 943-949.
32. Musacchio, T., Laquintana, V., Latrofa, A., Trapani, G., Torchilin, V. P., PEG-PE micelles loaded with paclitaxel and surface-modified by a PBR-ligand: Synergistic anticancer effect. Mol. Pharm. 2009, 6, 468-479.
33. Gill, K. K., Kaddoumi, A., Nazzal, S., Mixed micelles of PEG 2000-DSPE and vitamin-E TPGS for concurrent delivery of paclitaxel and parthenolide: Enhanced chemosenstization and antitumor efficacy against non-small cell lung cancer (NSCLC) cell lines. Eur. J. Pharm. Sci. 2012, 46, 64-71.
34. Yao, H.-J., Ju, R.-J., Wang, X.-X., Zhang, Y. et al., The antitumor efficacy of functional paclitaxel nanomicelles in treating resistant breast cancers by oral delivery. Biomaterials 2011, 32, 3285-3302.
35. Gruber, H. J., Hahn, C. D., Kada, G., Riener, C. K. et al., Anomalous fluorescence enhancement of Cy3 and Cy3.5 versus anomalous fluorescence loss of Cy5 and Cy7 upon covalent linking to IgG and noncovalent binding to avidin. Bioconjug. Chem. 2000, 11, 696-704.
36. Arik, M., Celebi, N., Onganer, Y., Fluorescence quenching of fluorescein with molecular oxygen in solution. J. Photochem. Photobiol. A 2005, 170, 7-7.
37. Chen, R. F., Knutson, J. R., Mechanism of fluorescence concentration quenching of carboxyfluorescein in liposomes: Energy transfer to nonfluorescent dimmers. Anal. Biochem. 1988, 172, 61-77.
38. Rhaese, S., von Briesen, H., Rübsamen-Waigmann, H., Kreuter, J., Langer, K., Human serum albumin-polyethylenimine nanoparticles for gene delivery. J. Control. Release 2003, 92, 199-208.
39. Rejman, J., Oberle, V., Zuhorn, I. S., Hoekstra, D., Sizedependent internalization of particles via the pathways of clathrin-and caveolae-mediated endocytosis. Biochem. J. 2004, 377, 159-169.
40. Sawant, R. R., Torchilin, V. P., Enhanced cytotoxicity of TATp-bearing paclitaxel-loaded micelles in vitro and in vivo. Int. J. Pharm. 2009, 374, 114-118.
41. Mitchell, D. J., Kim, D. T., Steinman, L., Fathman, C. G., Rothbard, J. B., Polyarginine enters cells more efficiently than other polycationic homopolymers. J. Pept. Res. 2000, 56, 318-325.
42. Torchilin, V. P., Recent approaches to intracellular delivery of drugs and DNA and organelle targeting. Annu Rev. Biomed. Eng. 2006, 8, 343-375.
43. Nel, A. E., Mädler, L., Velegol, D., Xia, T. et al., Understanding biophysicochemical interactions at the nano-bio interface. Nature 2009, 8, 543-557.
44. Jordan, M. A., Wilson, L., Microtubules as a target for anticancer drugs. Nat. Rev. Cancer 2004, 4, 253-265.
45. Torchilin, V. P., Fluorescence microscopy to follow the targeting of liposomes and micelles to cells and their intracellular fate. Adv Drug Deliv Rev. 2005, 57, 95-109.