The importance of endo-lysosomal escape with lipid nanocapsules for drug subcellular bioavailability

Biomaterials

Volumn 31, Issue 29, 2010, Pages 7542-7554

  Paillard, Archibald ^a   Hindré, François ^a   Vignes Colombeix, Caroline ^b   Benoit, Jean Pierre ^a   Garcion, Emmanuel ^a  

^a UNIVERSITÉ D'ANGERS   (France)

^b UNIVERSITÉ DE NANTES   (France)

Author keywords

Cancer therapy; Intracellular drug delivery; Nanoparticles; Subcellular trafficking; Surfactant

Indexed keywords

BIOCHEMISTRY; CELL DEATH; HYDRAULIC STRUCTURES; MICROEMULSIONS; MOLECULAR BIOLOGY; NANOCAPSULES; NANOPARTICLES; POLYETHYLENE GLYCOLS; SURFACE ACTIVE AGENTS;

BIOLOGICAL STRUCTURES; CANCER THERAPY; INTRACELLULAR DRUG DELIVERY; INTRACELLULAR TRAFFICKING; LYSOSOMAL DEGRADATION; PHASE INVERSION PROCESS; SUBCELLULAR TRAFFICKING; V-ATPASE INHIBITORS;

DRUG DELIVERY;

LIPID; NANOCAPSULE; PACLITAXEL; TECHNETIUM 99M;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL COMPARTMENTALIZATION; CELL DEATH; CELL MIGRATION; CELL SURVIVAL; CONCENTRATION RESPONSE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG BIOAVAILABILITY; DRUG DELIVERY SYSTEM; DRUG TRANSPORT; ENDOCYTOSIS; FLOW CYTOMETRY; GLIOMA CELL; ISOTOPE LABELING; LYSOSOME; MOUSE; NEWBORN; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

RATTUS;

EID: 77955278059     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2010.06.024     Document Type: Article

References (66)

1. Moghimi S.M., Hunter A.C., Murray J.C. Nanomedicine: current status and future prospects. Faseb J 2005, 19:311-330.
2. Peer D., Karp J.M., Hong S., Farokhzad O.C., Margalit R., Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007, 2:751-760.
3. Panyam J., Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev 2003, 55:329-347.
4. Torchilin V.P. Recent approaches to intracellular delivery of drugs and DNA and organelle targeting. Annu Rev Biomed Eng 2006, 8:343-375.
5. Pelkmans L., Helenius A. Insider information: what viruses tell us about endocytosis. Curr Opin Cell Biol 2003, 15:414-422.
6. Johannes L., Lamaze C. Clathrin-dependent or not: is it still the question?. Traffic 2002, 3:443-451.
7. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
8. Mercer J., Helenius A. Virus entry by macropinocytosis. Nat Cell Biol 2009, 11:510-520.
9. Nabi I.R., Le P.U. Caveolae/raft-dependent endocytosis. J Cell Biol 2003, 161:673-677.
10. Glebov O.O., Bright N.A., Nichols B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nat Cell Biol 2006, 8:46-54.
11. Rejman J., Oberle V., Zuhorn I.S., Hoekstra D. Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 2004, 377:159-169.
12. Prabha S., Zhou W.Z., Panyam J., Labhasetwar V. Size-dependency of nanoparticle-mediated gene transfection: studies with fractionated nanoparticles. Int J Pharm 2002, 244:105-115.
13. Zauner W., Farrow N.A., Haines A.M. In vitro uptake of polystyrene microspheres: effect of particle size, cell line and cell density. J Control Release 2001, 71:39-51.
14. Nichols B. Caveosomes and endocytosis of lipid rafts. J Cell Sci 2003, 116:4707-4714.
15. Dunn K.W., Maxfield F.R. Delivery of ligands from sorting endosomes to late endosomes occurs by maturation of sorting endosomes. J Cell Biol 1992, 117:301-310.
16. Lakadamyali M., Rust M.J., Zhuang X. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 2006, 124:997-1009.
17. Panyam J., Zhou W.Z., Prabha S., Sahoo S.K., Labhasetwar V. Rapid endo-lysosomal escape of poly(dl-lactide-co-glycolide) nanoparticles: implications for drug and gene delivery. Faseb J 2002, 16:1217-1226.
18. Harush-Frenkel O., Rozentur E., Benita S., Altschuler Y. Surface charge of nanoparticles determines their endocytic and transcytotic pathway in polarized MDCK cells. Biomacromolecules 2008, 9:435-443.
19. Sasaki K., Kogure K., Chaki S., Nakamura Y., Moriguchi R., Hamada H., et al. An artificial virus-like nano carrier system: enhanced endosomal escape of nanoparticles via synergistic action of pH-sensitive fusogenic peptide derivatives. Anal Bioanal Chem 2008, 391:2717-2727.
20. Zelphati O., Szoka F.C. Mechanism of oligonucleotide release from cationic liposomes. Proc Natl Acad Sci U S A 1996, 93:11493-11498.
21. Akinc A., Thomas M., Klibanov A.M., Langer R. Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis. J Gene Med 2005, 7:657-663.
22. Rozema D.B., Lewis D.L., Wakefield D.H., Wong S.C., Klein J.J., Roesch P.L., et al. Dynamic polyconjugates for targeted in vivo delivery of siRNA to hepatocytes. Proc Natl Acad Sci U S A 2007, 104:12982-12987.
23. Heurtault B., Saulnier P., Pech B., Proust J.E., Benoit J.P. A novel phase inversion-based process for the preparation of lipid nanocarriers. Pharm Res 2002, 19:875-880.
24. Heurtault B., Saulnier P., Pech B., Venier-Julienne M.C., Proust J.E., Phan-Tan-Luu R., et al. The influence of lipid nanocapsule composition on their size distribution. Eur J Pharm Sci 2003, 18:55-61.
25. Beduneau A., Saulnier P., Anton N., Hindre F., Passirani C., Rajerison H., et al. Pegylated nanocapsules produced by an organic solvent-free method: evaluation of their stealth properties. Pharm Res 2006, 23:2190-2199.
26. Ballot S., Noiret N., Hindre F., Denizot B., Garin E., Rajerison H., et al. 99mTc/188Re-labeled lipid nanocapsules as promising radiotracers for imaging and therapy: formulation and biodistribution. Eur J Nucl Med Mol Imaging 2006, 33:602-607.
27. Garcion E., Lamprecht A., Heurtault B., Paillard A., Aubert-Pouessel A., Denizot B., et al. A new generation of anticancer, drug-loaded, colloidal vectors reverses multidrug resistance in glioma and reduces tumor progression in rats. Mol Cancer Ther 2006, 5:1710-1722.
28. Allard E., Passirani C., Garcion E., Pigeon P., Vessieres A., Jaouen G., et al. Lipid nanocapsules loaded with an organometallic tamoxifen derivative as a novel drug-carrier system for experimental malignant gliomas. J Control Release 2008, 130:146-153.
29. Mevellec F., Tisato F., Refosco F., Roucoux A., Noiret N., Patin H., et al. Synthesis and characterization of the " sulfur-rich" bis(perthiobenzoato)(dithiobenzoato)technetium(III) heterocomplex. Inorg Chem 2002, 41:598-601.
30. Lacoeuille F., Hindre F., Moal F., Roux J., Passirani C., Couturier O., et al. In vivo evaluation of lipid nanocapsules as a promising colloidal carrier for paclitaxel. Int J Pharm 2007, 344:143-149.
31. Douliez J.P., Navailles L., Nallet F., Gaillard C. Self-assembly of unprecedented swollen multilamellar twisted ribbons from a racemic hydroxy fatty acid. Chemphyschem 2008, 9:74-77.
32. McCarthy K.D., de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 1980, 85:890-902.
33. Rodal S.K., Skretting G., Garred O., Vilhardt F., van Deurs B., Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 1999, 10:961-974.
34. Larkin J.M., Brown M.S., Goldstein J.L., Anderson R.G. Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts. Cell 1983, 33:273-285.
35. Liu N.Q., Lossinsky A.S., Popik W., Li X., Gujuluva C., Kriederman B., et al. Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway. J Virol 2002, 76:6689-6700.
36. Goncalves C., Mennesson E., Fuchs R., Gorvel J.P., Midoux P., Pichon C. Macropinocytosis of polyplexes and recycling of plasmid via the clathrin-dependent pathway impair the transfection efficiency of human hepatocarcinoma cells. Mol Ther 2004, 10:373-385.
37. Vercauteren D., Vandenbroucke R.E., Jones A.T., Rejman J., Demeester J., De Smedt S.C., et al. The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Mol Ther 2010, 18:561-569.
38. Zang Y., Beard R.L., Chandraratna R.A., Kang J.X. Evidence of a lysosomal pathway for apoptosis induced by the synthetic retinoid CD437 in human leukemia HL-60 cells. Cell Death Differ 2001, 8:477-485.
39. LaManna J.C. Intracellular pH determination by absorption spectrophotometry of neutral red. Metab Brain Dis 1987, 2:167-182.
40. Tomoda H., Kishimoto Y., Lee Y.C. Temperature effect on endocytosis and exocytosis by rabbit alveolar macrophages. J Biol Chem 1989, 264:15445-15450.
41. Hed J., Hallden G., Johansson S.G., Larsson P. The use of fluorescence quenching in flow cytofluorometry to measure the attachment and ingestion phases in phagocytosis in peripheral blood without prior cell separation. J Immunol Methods 1987, 101:119-125.
42. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc Natl Acad Sci U S A 1999, 96:6775-6780.
43. Huss M., Ingenhorst G., Konig S., Gassel M., Drose S., Zeeck A., et al. Concanamycin A, the specific inhibitor of V-ATPases, binds to the V(o) subunit c. J Biol Chem 2002, 277:40544-40548.
44. Verma A., Uzun O., Hu Y., Han H.S., Watson N., Chen S., et al. Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles. Nat Mater 2008, 7:588-595.
45. Kunisawa J., Masuda T., Katayama K., Yoshikawa T., Tsutsumi Y., Akashi M., et al. Fusogenic liposome delivers encapsulated nanoparticles for cytosolic controlled gene release. J Control Release 2005, 105:344-353.
46. Huwyler J., Wu D., Pardridge W.M. Brain drug delivery of small molecules using immunoliposomes. Proc Natl Acad Sci U S A 1996, 93:14164-14169.
47. Roger E., Lagarce F., Garcion E., Benoit J.P. Lipid nanocarriers improve paclitaxel transport throughout human intestinal epithelial cells by using vesicle-mediated transcytosis. J Control Release 2009, 140:174-181.
48. Lai S.K., Hida K., Man S.T., Chen C., Machamer C., Schroer T.A., et al. Privileged delivery of polymer nanoparticles to the perinuclear region of live cells via a non-clathrin, non-degradative pathway. Biomaterials 2007, 28:2876-2884.
49. Ruckert P., Bates S.R., Fisher A.B. Role of clathrin- and actin-dependent endocytotic pathways in lung phospholipid uptake. Am J Physiol Lung Cell Mol Physiol 2003, 284:L981-L989.
50. Luhmann T., Rimann M., Bittermann A.G., Hall H. Cellular uptake and intracellular pathways of PLL-g-PEG-DNA nanoparticles. Bioconjug Chem 2008, 19:1907-1916.
51. Joo K.I., Lei Y., Lee C.L., Lo J., Xie J., Hamm-Alvarez S.F., et al. Site-specific labeling of enveloped viruses with quantum dots for single virus tracking. ACS Nano 2008, 2:1553-1562.
52. Ghosh R.N., Gelman D.L., Maxfield F.R. Quantification of low density lipoprotein and transferrin endocytic sorting HEp2 cells using confocal microscopy. J Cell Sci 1994, 107(Pt 8):2177-2189.
53. Hopkins C.R., Gibson A., Shipman M., Miller K. Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 1990, 346:335-339.
54. Zerial M., McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001, 2:107-117.
55. Steinman R.M., Mellman I.S., Muller W.A., Cohn Z.A. Endocytosis and the recycling of plasma membrane. J Cell Biol 1983, 96:1-27.
56. Panyam J., Labhasetwar V. Dynamics of endocytosis and exocytosis of poly(D, L-lactide-co-glycolide) nanoparticles in vascular smooth muscle cells. Pharm Res 2003, 20:212-220.
57. Nam H.Y., Kwon S.M., Chung H., Lee S.Y., Kwon S.H., Jeon H., et al. Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. J Control Release 2009, 135:259-267.
58. Felgner J.H., Kumar R., Sridhar C.N., Wheeler C.J., Tsai Y.J., Border R., et al. Enhanced gene delivery and mechanism studies with a novel series of cationic lipid formulations. J Biol Chem 1994, 269:2550-2561.
59. Ng C.P., Goodman T.T., Park I.K., Pun S.H. Bio-mimetic surface engineering of plasmid-loaded nanoparticles for active intracellular trafficking by actin comet-tail motility. Biomaterials 2009, 30:951-958.
60. Dubowchik G.M., Gawlak S.L., Firestone R.A. The in vitro effects of three lysosomotropic detergents against three human tumor cell lines. Bioorg Med Chem Lett 1995, 5:893-898.
61. Ouar Z., Bens M., Vignes C., Paulais M., Pringel C., Fleury J., et al. Inhibitors of vacuolar H+-ATPase impair the preferential accumulation of daunomycin in lysosomes and reverse the resistance to anthracyclines in drug-resistant renal epithelial cells. Biochem J 2003, 370:185-193.
62. Roger E., Lagarce F., Garcion E., Benoit J.P. Reciprocal competition between lipid nanocapsules and p-gp for paclitaxel transport across caco-2 cells. Eur J Pharm Sci 2010, 40:422-429.
63. Rammer P., Groth-Pedersen L., Kirkegaard T., Daugaard M., Rytter A., Szyniarowski P., et al. BAMLET activates a lysosomal cell death program in cancer cells. Mol Cancer Ther 2010, 9:24-32.
64. Ostenfeld M.S., Hoyer-Hansen M., Bastholm L., Fehrenbacher N., Olsen O.D., Groth-Pedersen L., et al. Anti-cancer agent siramesine is a lysosomotropic detergent that induces cytoprotective autophagosome accumulation. Autophagy 2008, 4:487-499.
65. Lacoeuille F., Garcion E., Benoit J.P., Lamprecht A. Lipid nanocapsules for intracellular drug delivery of anticancer drugs. J Nanosci Nanotechnol 2007, 7:4612-4617.
66. Schiff P.B., Horwitz S.B. Taxol stabilizes microtubules in mouse fibroblast cells. Proc Natl Acad Sci U S A 1980, 77:1561-1565.