Endocytosis of nanomedicines

Journal of Controlled Release

Volumn 145, Issue 3, 2010, Pages 182-195

  Sahay, Gaurav ^a   Alakhova, Daria Y ^a   Kabanov, Alexander V ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

Caveolae; Clathrin; Endocytosis; Intracellular trafficking; Nanomedicines; Nanoparticles

Indexed keywords

CAVEOLAE; CELL INTERACTION; CELL TYPES; CELLULAR RESPONSE; CLATHRINS; IMAGING AGENT; INTRACELLULAR TRAFFICKING; MATERIAL COMPOSITIONS; MULTIPLE PATHWAYS; NANO-MATERIALS; NANOMATERIAL; NANOMEDICINES; SITE-SPECIFIC; SUB-CELLULAR; TARGET CELLS; THERAPEUTIC NANOMATERIALS;

ANTIGEN-ANTIBODY REACTIONS; CELL MEMBRANES; CYTOLOGY; DISEASE CONTROL; DRUG THERAPY; NANOPARTICLES; NANOSTRUCTURED MATERIALS; SURFACE CHEMISTRY;

DIAGNOSIS;

CHITOSAN; CLATHRIN; DOXORUBICIN; LIPOPLEX; MACROGOL; NANOMATERIAL; PACLITAXEL; POLOXAMER; POLYAMIDOAMINE; POLYGLACTIN; POLYSILOXANE; QUANTUM DOT; SILICON DIOXIDE;

CAVEOLA; CELL ACTIVITY; CELL INTERACTION; CELL TYPE; DRUG DELIVERY SYSTEM; DRUG FORMULATION; ENDOCYTOSIS; HUMAN; MICELLE; NANOMEDICINE; NONHUMAN; PARTICLE SIZE; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; REVIEW; TARGET CELL; ANIMAL; CHEMISTRY; PROCEDURES;

ANIMALS; ENDOCYTOSIS; HUMANS; NANOMEDICINE; NANOSTRUCTURES;

EID: 77954214896     PISSN: 01683659     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jconrel.2010.01.036     Document Type: Review

References (119)

1. Kabanov A.V., Alakhov V.Y. Pluronic (R) block copolymers in drug delivery: from micellar nanocontainers to biological response modifiers. Critical Reviews in Therapeutic Drug Carrier Systems 2002, 19:1-72.
2. Duncan R. The dawning era of polymer therapeutics. Nature Review Drug Discovery 2003, 2:347-360.
3. Farokhzad O.C., Langer R. Nanomedicine: developing smarter therapeutic and diagnostic modalities. Advanced Drug Delivery Reviews 2006, 58:1456-1459.
4. Davis M.E., Chen Z., Shin D.M. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nature Review Drug Discovery 2008, 7:771-782.
5. Peer D., Karp J.M., Hong S., Farokhzad O.C., Margalit R., Langer R. Nanocarriers as an emerging platform for cancer therapy. Nature Nanotechnology 2007, 2:751-760.
6. Tasciotti E., Liu X., Bhavane R., Plant K., Leonard A.D., Price B.K., Cheng M.M.-C., Decuzzi P., Tour J.M., Robertson F., Ferrari M. Mesoporous silicon particles as a multistage delivery system for imaging and therapeutic applications. Nature Nanotechnology 2008, 3:151-157.
7. Rajendran L., Knolker H.-J., Simons K. Subcellular targeting strategies for drug design and delivery. Nature Review Drug Discovery 2010, 9:29-42.
8. Germain R.N. An innately interesting decade of research in immunology. Nature Medicine 2004, 10:1307-1320.
9. Conner S.D., Schmid S.L. Regulated portals of entry into the cell. Nature 2003, 422:37-44.
10. Mayor S., Pagano R.E. Pathways of clathrin-independent endocytosis. Nature Review Molecular Cell Biology 2007, 8:603-612.
11. Wieffer M., Maritzen T., Haucke V. SnapShot: endocytic trafficking. Cell 2009, 137:382.e381-382.e383.
12. Doherty G.J., McMahon H.T. Mechanisms of endocytosis. Annual Review of Biochemistry 2009, 78:857.
13. Zerial M., McBride H. Rab proteins as membrane organizers. Nature Review Molecular Cell Biology 2001, 2:107-117.
14. Glebov O.O., Bright N.A., Nichols B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nature Cell Biology 2006, 8:46-54.
15. Storrie B., White J., Rottger S., Stelzer E.H.K., Suganuma T., Nilsson T. Recycling of Golgi-resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering. Journal of Cell Biology 1998, 143:1505-1521.
16. Falcon-Perez J.M., Nazarian R., Sabatti C., Dell'Angelica E.C. Distribution and dynamics of Lamp1-containing endocytic organelles in fibroblasts deficient in BLOC-3. Journal of Cell Science 2005, 118:5243-5255.
17. Fliegel L., Burns K., MacLennan D.H., Reithmeier R.A., Michalak M. Molecular cloning of the high affinity calcium-binding protein (calreticulin) of skeletal muscle sarcoplasmic reticulum. Journal of Biological Chemistry 1989, 264:21522-21528.
18. Hanson G.T., Aggeler R., Oglesbee D., Cannon M., Capaldi R.A., Tsien R.Y., Remington S.J. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. Journal of Biological Chemistry 2004, 279:13044-13053.
19. Kabouridis P.S., Magee A.I., Ley S.C. S-acylation of LCK protein tyrosine kinase is essential for its signalling function in T lymphocytes. The European Molecular Biology Organization Journal 1997, 16:4983-4998.
20. Straight A.F., Marshall W.F., Sedat J.W., Murray A.W. Mitosis in living budding yeast: anaphase a but no metaphase plate. Science 1997, 277:574-578.
21. Sahay G., Gautam V., Luxenhofer R., Kabanov A. The utilization of pathogen-like cellular trafficking by single chain block copolymer. Biomaterials 2009, Dec 4 Electronic publication ahead of print.
22. Oh P., Borgstrom P., Witkiewicz H., Li Y., Borgstrom B.J., Chrastina A., Iwata K., Zinn K.R., Baldwin R., Testa J.E., Schnitzer J.E. Live dynamic imaging of caveolae pumping targeted antibody rapidly and specifically across endothelium in the lung. Nature Biotechnology 2007, 25:327-337.
23. Vasir J.K., Labhasetwar V. Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. Biomaterials 2008, 29:4244-4252.
24. Mercer J., Helenius A. Virus entry by macropinocytosis. Nature Cell Biology 2009, 11:510-520.
25. A.I. Ivanov, Pharmacological Inhibition of Endocytic Pathways: Is It Specific Enough to Be Useful?, Methods in Molecular Biology 2008, Review.
26. Sahay G., Kim J.O., Kabanov A.V., Bronich T.K. The exploitation of differential endocytic pathways in normal and tumor cells in the selective targeting of nanoparticulate chemotherapeutic agents. Biomaterials Feb 2010, 31(5):923-933.
27. Tuli A., Sharma M., Capek H.L., Naslavsky N., Caplan S., Solheim J.C. Mechanism for amyloid precursor-like protein 2 enhancement of major histocompatibility complex class I molecule degradation. Journal of Biological Chemistry Dec 4 2009, 284(49):34296-34307.
28. Damm E.-M., Pelkmans L., Kartenbeck J., Mezzacasa A., Kurzchalia T., Helenius A. Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. Journal of Cell Biology 2005, 168:477-488.
29. Gumbleton M., Stephens D.J. Coming out of the dark: the evolving role of fluorescence imaging in drug delivery research. Advanced Drug Delivery Reviews 2005, 57:5-15.
30. Lai S.K., Hanes J. Real-time multiple particle tracking of gene nanocarriers in complex biological environments. Methods in Molecular Biology 2008, 434:81-97.
31. Hillaireau H., Couvreur P. Nanocarriers' entry into the cell: relevance to drug delivery. Cellular and Molecular Life Sciences 2009, 66:2873-2896.
32. Aderem A., Underhill D.M. Mechanisms of phagocytosis in macrophages. Annual Review of Immunology 1999, 17:593-623.
33. Rabinovitch M. Professional and nonprofessional phagocytes-an introduction. Trends in Cell Biology 1995, 5:85-87.
34. Cannon G., Swanson J. The macrophage capacity for phagocytosis. Journal of Cell Sciences 1992, 101:907-913.
35. Champion J.A., Katare Y.K., Mitragotri S. Making polymeric micro- and nanoparticles of complex shapes. Proceedings of the National Academy of Sciences 2007, 104:11901-11904.
36. Champion J.A., Mitragotri S. Role of target geometry in phagocytosis. Proceedings of the National Academy of Sciences 2006, 103:4930-4934.
37. Pucadyil T.J., Schmid S.L. Conserved functions of membrane active GTPases in coated vesicle formation. Science 2009, 325:1217-1220.
38. Slepnev V.I., De Camilli P. Accessory factors in clathrin-dependent synaptic vesicle endocytosis. Nature Review Neuroscience 2000, 1:161-172.
39. Ford M.G.J., Mills I.G., Peter B.J., Vallis Y., Praefcke G.J.K., Evans P.R., McMahon H.T. Curvature of clathrin-coated pits driven by epsin. Nature 2002, 419:361-366.
40. Rappoport J.Z. Focusing on clathrin-mediated endocytosis. Biochemical Journal 2008, 412:415-423.
41. Harush-Frenkel O., Debotton N., Benita S., Altschuler Y. Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochemical and Biophysical Research Communications 2007, 353:26-32.
42. 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.
43. Lahtinen U., Honsho M., Parton R.G., Simons K., Verkade P. Involvement of caveolin-2 in caveolar biogenesis in MDCK cells. Federation of the Societies of Biochemistry and Molecular Biology Letters 2003, 538:85-88.
44. Vogel U., Sandvig K., van Deurs B. Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCK II cells. Journal of Cell Science 1998, 111:825-832.
45. Lü J.-M., Wang X., Marin-Muller C., Wang H., Lin P.H., Yao Q., Chen C. Current advances in research and clinical applications of PLGA-based nanotechnology. Expert Review of Molecular Diagnostics 2009, 9:325-341.
46. Panyam J., Labhasetwar V. Dynamics of endocytosis and exocytosis of Poly(d, l-lactide-co-Glycolide) nanoparticles in vascular smooth muscle cells. Pharmaceutical Research 2003, 20:212-220.
47. Qaddoumi M.G., Ueda H., Yang J., Davda J., Labhasetwar V., Lee V.H. The characteristics and mechanisms of uptake of PLGA nanoparticles in rabbit conjunctival epithelial cell layers. Pharmaceutical Research 2004, 21:641-648.
48. Nan A., Bai X., Son S.J., Lee S.B., Ghandehari H. Cellular uptake and cytotoxicity of silica nanotubes. Nano Letters 2008, 8:2150-2154.
49. Chung T.-H., Wu S.-H., Yao M., Lu C.-W., Lin Y.-S., Hung Y., Mou C.-Y., Chen Y.-C., Huang D.-M. The effect of surface charge on the uptake and biological function of mesoporous silica nanoparticles in 3T3-L1 cells and human mesenchymal stem cells. Biomaterials 2007, 28:2959-2966.
50. Ma Z., Lim L.-Y. Uptake of chitosan and associated insulin in caco-2 cell monolayers: a comparison between chitosan molecules and chitosan nanoparticles. Pharmaceutical Research 2003, 20:1812-1819.
51. Huang M., Ma Z., Khor E., Lim L.-Y. Uptake of FITC-chitosan nanoparticles by A549 cells. Pharmaceutical Research 2002, 19:1488-1494.
52. Nam H.Y., Kwon S.M., Chung H., Lee S.-Y., Kwon S.-H., Jeon H., Kim Y., Park J.H., Kim J., Her S., Oh Y.-K., Kwon I.C., Kim K., Jeong S.Y. Cellular uptake mechanism and intracellular fate of hydrophobically modified glycol chitosan nanoparticles. Journal of Controlled Release 2009, 135:259-267.
53. Bareford L.M., Swaan P.W. Endocytic mechanisms for targeted drug delivery. Advanced Drug Delivery Reviews 2007, 59:748-758.
54. Tekle C., Deurs B.v., Sandvig K., Iversen T.-G. Cellular trafficking of quantum dot-ligand bioconjugates and their induction of changes in normal routing of unconjugated ligands. Nano Letters 2008, 8:1858-1865.
55. Sahay G., Batrakova E.V., Kabanov A.V. Different internalization pathways of polymeric micelles and unimers and their effects on vesicular transport. Bioconjugate Chemistry 2008, 19:2023-2029.
56. Simons K., Toomre D. Lipid rafts and signal transduction. Nature Review Molecular Cell Biology 2000, 1:31-39.
57. Nabi I.R. Cavin fever: regulating caveolae. Nature Cell Biology 2009, 11:789-791.
58. Schnitzer J.E., Liu J., Oh P. Endothelial caveolae have the molecular transport machinery for vesicle budding, docking, and fusion including VAMP, NSF, SNAP, annexins, and GTPases. Journal of Biological Chemistry 1995, 270:14399-14404.
59. Parton R.G., Simons K. The multiple faces of caveolae. Nature Review Molecular Cell Biology 2007, 8:185-194.
60. Carver L.A., Schnitzer J.E. Caveolae: mining little caves for new cancer targets. Nature Review Cancer 2003, 3:571-581.
61. Rejman J., Conese M., Hoekstra D. Gene transfer by means of lipo- and polyplexes: role of clathrin and caveolae-mediated endocytosis. Journal of Liposome Research 2006, 16:237-247.
62. Garcia-Cardena G., Oh P., Liu J., Schnitzer J.E., Sessa W.C. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proceedings of National Academy of Science U S A 1996, 93:6448-6453.
63. Bronich T.K., Keifer P.A., Shlyakhtenko L.S., Kabanov A.V. Polymer micelle with cross-linked ionic core. Journal of the American Chemical Society 2005, 127:8236-8237.
64. Nishikawa T., Iwakiri N., Kaneko Y., Taguchi A., Fukushima K., Mori H., Morone N., Kadokawa J.-i. Nitric oxide release in human aortic endothelial cells mediated by delivery of amphiphilic polysiloxane nanoparticles to caveolae. Biomacromolecules 2009, 10:2074-2085.
65. Zhang L.W., Monteiro-Riviere N.A. Mechanisms of quantum dot nanoparticle cellular uptake. Toxicological Sciences 2009, 110:138-155.
66. Moreno-Aspitia A., Perez E.A. Nanoparticle albumin-bound paclitaxel (ABI-007): a newer taxane alternative in breast cancer. Future Oncology 2005, 1:755-762.
67. Gradishar W.J. Albumin-bound paclitaxel: a next-generation taxane. Expert Opinion on Pharmacotherapy 2006, 7:1041.
68. Schnitzer J.E. gp60 is an albumin-binding glycoprotein expressed by continuous endothelium involved in albumin transcytosis. American Journal of Physiology, Heart and Circulatory Physiology 1992, 262:H246-H254.
69. Desai N.P., Trieu V., Hwang L.Y., Wu R.J., Soon-Shiong P., Gradishar W.J. Improved effectiveness of nanoparticle albumin-bound (nab) paclitaxel versus polysorbate-based docetaxel in multiple xenografts as a function of HER2 and SPARC status. Anti-Cancer Drugs 2008, 19:899-909.
70. Gradishar W.J. Albumin-bound paclitaxel: a next-generation taxane. Expert Opinion on Pharmacotherapy 2006, 7:1041-1053.
71. Oba M., Aoyagi K., Miyata K., Matsumoto Y., Itaka K., Nishiyama N., Yamasaki Y., Koyama H., Kataoka K. Polyplex micelles with cyclic rgd peptide ligands and disulfide cross-links directing to the enhanced transfection via controlled intracellular trafficking. Molecular Pharmaceutics 2008, 5:1080-1092.
72. Larson D.R., Gosse J.A., Holowka D.A., Baird B.A., Webb W.W. Temporally resolved interactions between antigen-stimulated IgE receptors and Lyn kinase on living cells. Journal of Cell Biology 2005, 171:527-536.
73. Sabharanjak S., Sharma P., Parton R.G., Mayor S. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Developmental Cell 2002, 2:411-423.
74. Tuli A., Sharma M., McIlhaney M.M., Talmadge J.E., Naslavsky N., Caplan S., Solheim J.C. Amyloid precursor-like protein 2 increases the endocytosis, instability, and turnover of the H2-Kd MHC class i molecule. Journal of Immunology 2008, 181:1978-1987.
75. Lu Y., Low P.S. Folate-mediated delivery of macromolecular anticancer therapeutic agents. Advanced Drug Delivery Reviews 2002, 54:675-693.
76. Rijnboutt S., Jansen G., Posthuma G., Hynes J., Schornagel J., Strous G. Endocytosis of GPI-linked membrane folate receptor-alpha. Journal of Cell Biology 1996, 132:35-47.
77. Kerr M.C., Teasdale R.D. Defining macropinocytosis. Traffic 2009, 10:364-371.
78. Jones A.T. Macropinocytosis: searching for an endocytic identity and role in the uptake of cell penetrating peptides. Journal of Cellular and Molecular Medicine 2007, 11:670-684.
79. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nature Review Molecular Cell Biology 2008, 9:639-649.
80. Gratton S.E.A., Williams S.S., Napier M.E., Pohlhaus P.D., Zhou Z., Wiles K.B., Maynor B.W., Shen C., Olafsen T., Samulski E.T., DeSimone J.M. The pursuit of a scalable nanofabrication platform for use in material and life science applications. Accounts of Chemical Research 2008, 41:1685-1695.
81. Gratton S.E.A., Ropp P.A., Pohlhaus P.D., Luft J.C., Madden V.J., Napier M.E., DeSimone J.M. The effect of particle design on cellular internalization pathways. Proceedings of the National Academy of Sciences 2008, 105:11613-11618.
82. Batrakova E.V., Kabanov A.V. Pluronic block copolymers: evolution of drug delivery concept from inert nanocarriers to biological response modifiers. Journal of Controlled Release 2008, 130:98-106.
83. Lai S.K., Hida K., Chen C., Hanes J. Characterization of the intracellular dynamics of a non-degradative pathway accessed by polymer nanoparticles. Journal of Controlled Release 2008, 125:107-111.
84. Esfand R., Tomalia D.A. Poly(amidoamine) (PAMAM) dendrimers: from biomimicry to drug delivery and biomedical applications. Drug Discovery Today 2001, 6:427-436.
85. Kitchens K., Foraker A., Kolhatkar R., Swaan P., Ghandehari H. Endocytosis and interaction of Poly (Amidoamine) dendrimers with Caco-2 cells. Pharmaceutical Research 2007, 24:2138-2145.
86. Seib F.P., Jones A.T., Duncan R. Comparison of the endocytic properties of linear and branched PEIs, and cationic PAMAM dendrimers in B16f10 melanoma cells. Journal of Controlled Release 2007, 117:291-300.
87. Kitchens K.M., Kolhatkar R.B., Swaan P.W., Ghandehari H. Endocytosis inhibitors prevent Poly(amidoamine) dendrimer internalization and permeability across Caco-2 cells. Molecular Pharmaceutics 2008, 5:364-369.
88. Kitchens K., Kolhatkar R., Swaan P., Eddington N., Ghandehari H. Transport of Poly(Amidoamine) dendrimers across Caco-2 cell monolayers: influence of size. Charge and Fluorescent Labeling, Pharmaceutical Research 2006, 23:2818-2826.
89. Kabanov A.V., Kabanov V.A. DNA complexes with polycations for the delivery of genetic material into cells. Bioconjugate Chemistry 1995, 6:7-20.
90. von Gersdorff K., Sanders N.N., Vandenbroucke R., De Smedt S.C., Wagner E., Ogris M. The internalization route resulting in successful gene expression depends on both cell line and polyethylenimine polyplex type. Molecular Therapy 2006, 14:745-753.
91. Akinc A., Thomas M., Klibanov A.M., Langer R. Exploring polyethylenimine-mediated DNA transfection and the proton sponge hypothesis. The Journal of Gene Medicine 2005, 7:657-663.
92. Rejman J., Bragonzi A., Conese M. Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes. Molecular Therapy 2005, 12:468-474.
93. Yang Z., Sahay G., Sriadibhatla S., Kabanov A.V. Amphiphilic block copolymers enhance cellular uptake and nuclear entry of polyplex-delivered DNA. Bioconjugate Chemistry 2008, 19:1987-1994.
94. Lühmann T., Rimann M., Bittermann A.G., Hall H. Cellular uptake and intracellular pathways of PLL-g-PEG-DNA nanoparticles. Bioconjugate Chemistry 2008, 19:1907-1916.
95. Wong A.W., Scales S.J., Reilly D.E. DNA internalized via caveolae requires microtubule-dependent, Rab7-independent transport to the late endocytic pathway for delivery to the nucleus. Journal of Biological Chemistry 2007, 282:22953-22963.
96. Bausinger R., Gersdorff K.v., Braeckmans K., Ogris M., Wagner E., Bräuchle C., Zumbusch A. The transport of nanosized gene carriers unraveled by live-cell imaging13. Angewandte Chemie International Edition 2006, 45:1568-1572.
97. Suh J., Wirtz D., Hanes J. Efficient active transport of gene nanocarriers to the cell nucleus. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:3878-3882.
98. Boussif O., Lezoualc'h F., Zanta M.A., Mergny M.D., Scherman D., Demeneix B., Behr J.P. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proceedings of the National Academy of Sciences 1995, 92:7297-7301.
99. Miller A.M., Dean D.A. Tissue-specific and transcription factor-mediated nuclear entry of DNA. Advanced Drug Delivery Reviews 2009, 61:603-613.
100. Sriadibhatla S., Yang Z., Gebhart C., Alakhov V.Y., Kabanov A. Transcriptional activation of gene expression by pluronic block copolymers in stably and transiently transfected cells. Molecular Therapy 2006, 13:804-813.
101. Gaymalov Z.Z., Yang Z., Pisarev V.M., Alakhov V.Y., Kabanov A.V. The effect of the nonionic block copolymer pluronic P85 on gene expression in mouse muscle and antigen-presenting cells. Biomaterials 2009, 30:1232-1245.
102. Fumoto S., Nishi J., Ishii H., Wang X., Miyamoto H., Yoshikawa N., Nakashima M., Nakamura J., Nishida K. Rac-mediated macropinocytosis is a critical route for naked plasmid DNA transfer in mice. Molecular Pharmaceutics 2009, 6:1170-1179.
103. Wadia J.S., Dowdy S.F. Transmembrane delivery of protein and peptide drugs by TAT-mediated transduction in the treatment of cancer. Advanced Drug Delivery Reviews 2005, 57:579-596.
104. Torchilin V.P. Tat peptide-mediated intracellular delivery of pharmaceutical nanocarriers. Advanced Drug Delivery Reviews 2008, 60:548-558.
105. Kaplan I.M., Wadia J.S., Dowdy S.F. Cationic TAT peptide transduction domain enters cells by macropinocytosis. Journal of Controlled Release 2005, 102:247-253.
106. Wadia J.S., Stan R.V., Dowdy S.F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nature Medicine 2004, 10:310-315.
107. Patel L., Zaro J., Shen W.-C. Cell penetrating peptides: intracellular pathways and pharmaceutical perspectives. Pharmaceutical Research 2007, 24:1977-1992.
108. Sawant R.M., Hurley J.P., Salmaso S., Kale A., Tolcheva E., Levchenko T.S., Torchilin V.P. "SMART" drug delivery systems: double-targeted pH-responsive pharmaceutical nanocarriers. Bioconjugate Chemistry 2006, 17:943-949.
109. Kumar P., Wu H., McBride J.L., Jung K.-E., Hee Kim M., Davidson B.L., Kyung Lee S., Shankar P., Manjunath N. Transvascular delivery of small interfering RNA to the central nervous system. Nature 2007, 448:39-43.
110. Liu Y., Huang R., Han L., Ke W., Shao K., Ye L., Lou J., Jiang C. Brain-targeting gene delivery and cellular internalization mechanisms for modified rabies virus glycoprotein RVG29 nanoparticles. Biomaterials 2009, 30:4195-4202.
111. Liu J., Kopečková P., Bühler P., Wolf P., Pan H., Bauer H., Elsässer-Beile U., Kopeček J.i. Biorecognition and subcellular trafficking of hpma copolymer - anti-PSMA antibody conjugates by prostate cancer cells. Molecular Pharmaceutics 2009, 6:959-970.
112. Muro S., Garnacho C., Champion J.A., Leferovich J., Gajewski C., Schuchman E.H., Mitragotri S., Muzykantov V.R. Control of endothelial targeting and intracellular delivery of therapeutic enzymes by modulating the size and shape of ICAM-1-targeted carriers. Molecular Therapy 2008, 16:1450-1458.
113. Champion J., Mitragotri S. Shape induced inhibition of phagocytosis of polymer particles. Pharmaceutical Research 2009, 26:244-249.
114. Kabanov Alexander V., Vinogradov Serguei V. Nanogels as pharmaceutical carriers: finite networks of infinite capabilities. Angewandte Chemie International Edition 2009, 48:5418-5429.
115. Basu S., Harfouche R., Soni S., Chimote G., Mashelkar R.A., Sengupta S. Nanoparticle-mediated targeting of MAPK signaling predisposes tumor to chemotherapy. Proceedings of the National Academy of Sciences 2009, 106:7957-7961.
116. D.Y. Alakhova, N.Y. Rapoport, E.V. Batrakova, A.A. Timoshin, S. Li, D. Nicholls, V.Y. Alakhov, A.V. Kabanov, Differential metabolic responses to pluronic in MDR and non-MDR cells: A novel pathway for chemosensitization of drug resistant cancers, Journal of Controlled Release, In Press, Corrected Proof.
117. M. Capitani, M. Sallese, The KDEL receptor: New functions for an old protein, Federation of the Societies of Biochemistry and Molecular Biology Letters, In Press, Corrected Proof.
118. Sabharanjak S., Mayor S. Folate receptor endocytosis and trafficking. Advanced Drug Delivery Reviews 2004, 56:1099-1109.
119. Arima Y., Toda M., Iwata H. Complement activation on surfaces modified with ethylene glycol units. Biomaterials 2008, 29:551-560.