Multivalent Glycosylation of Fluorescent Gold Nanoclusters Promotes Increased Human Dendritic Cell Targeting via Multiple Endocytic Pathways

ACS Applied Materials and Interfaces

Volumn 7, Issue 37, 2015, Pages 20945-20956

  Le Guével, Xavier ^a   Perez Perrino, Monica ^b   Fernández, Tahia D ^c,d   Palomares, Francisca ^c,d   Torres, Maria José ^d   Blanca, Miguel ^d   Rojo, Javier ^b   Mayorga, Cristobalina ^c,d  

^a Institute of Biomedical Research in Malaga and BIONAND Nanomedicine Platform   (Spain)

^b INSTITUTO DE INVESTIGACIONES QUÍMICAS   (Spain)

^c Research Laboratory   (Spain)

^d UNIVERSITY OF MÁLAGA   (Spain)

Author keywords

cell uptake; dendritic cells; gold nanoclusters; mannose; targeting

Indexed keywords

CARBOHYDRATES; CHELATION; CYTOLOGY; FLUORESCENCE; GOLD; LIGANDS; NANOCLUSTERS; PROTEINS;

CELL UPTAKE; DENDRITIC CELLS; GOLD NANOCLUSTER; MANNOSE; TARGETING;

CELLS;

GOLD; METAL NANOPARTICLE; WATER;

CHEMISTRY; DENDRITIC CELL; DRUG EFFECTS; ENDOCYTOSIS; FLOW CYTOMETRY; FLUORESCENCE; GLYCOSYLATION; HUMAN; LIGHT RELATED PHENOMENA; METABOLISM; PARTICLE SIZE; PHOTON CORRELATION SPECTROSCOPY; SPECTROFLUOROMETRY; ULTRASTRUCTURE;

DENDRITIC CELLS; DYNAMIC LIGHT SCATTERING; ENDOCYTOSIS; FLOW CYTOMETRY; FLUORESCENCE; GLYCOSYLATION; GOLD; HUMANS; METAL NANOPARTICLES; OPTICAL PHENOMENA; PARTICLE SIZE; SPECTROMETRY, FLUORESCENCE; WATER;

EID: 84942279541     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b06541     Document Type: Article

References (70)

1. Cruz, L. J.; Tacken, P. J.; Fokkink, R.; Joosten, B.; Stuart, M. C.; Albericio, F.; Torensma, R.; Figdor, C. G. Targeted PLGA Nano- but not Microparticles specifically deliver Antigen to human Dendritic Cells via DC-SIGN In Vitro J. Controlled Release 2010, 144 (2) 118-126 10.1016/j.jconrel.2010.02.013
2. Marradi, M.; Chiodo, F.; García, I.; Penadés, S. Glyconanoparticles as Multifunctional and Multimodal Carbohydrate Systems Chem. Soc. Rev. 2013, 42 (11) 4728-4745 10.1039/c2cs35420a
3. Novak, N. Targeting Dendritic Cells in Allergen Immunotherapy Immunol. Allergy Clin. North Am. 2006, 26 (2) 307-319 10.1016/j.iac.2006.02.010
4. Abbas, A. K.; Sharpe, A. H. Dendritic Cells giveth and taketh away Nat. Immunol. 2005, 6 (3) 227-228 10.1038/ni0305-227
5. Mellman, I.; Steinman, R. M. Dendritic cells: Specialized and Regulated Antigen Processing Machines Cell 2001, 106 (3) 255-258 10.1016/S0092-8674(01)00449-4
6. Hubbell, J. A.; Thomas, S. N.; Swartz, M. A. Materials Engineering for Immunomodulation Nature 2009, 462 (7272) 449-460 10.1038/nature08604
7. Kim, J.; Mooney, D. J. In Vivo Modulation of Dendritic Cells by Engineered Materials: Towards new Cancer Vaccines Nano Today 2011, 6 (5) 466-477 10.1016/j.nantod.2011.08.005
8. Kreutz, M.; Tacken, P. J.; Figdor, C. G. Targeting Dendritic Cells - why bother? Blood 2013, 121 (15) 2836-2844 10.1182/blood-2012-09-452078
9. Dobrovolskaia, M. A.; McNeil, S. E. Immunological Properties of Engineered Nanomaterials Nat. Nanotechnol. 2007, 2 (8) 469-478 10.1038/nnano.2007.223
10. Klippstein, R.; Pozo, D. Nanotechnology-based Manipulation of Dendritic Cells for Enhanced Immunotherapy Strategies Nanomedicine 2010, 6 (4) 523-529 10.1016/j.nano.2010.01.001
11. Reddy, S. T.; Rehor, A.; Schmoekel, H. G.; Hubbell, J. A.; Swartz, M. A. In Vivo Targeting of Dendritic Cells in Lymph Nodes with poly(propylene sulfide) Nanoparticles J. Controlled Release 2006, 112 (1) 26-34 10.1016/j.jconrel.2006.01.006
12. Hirosue, S.; Kourtis, I. C.; van der Vlies, A. J.; Hubbell, J. A.; Swartz, M. A. Antigen Delivery to Dendritic Cells by poly(propylene sulfide) Nanoparticles with disulfide Conjugated Peptides: Cross-Presentation and T cell Activation Vaccine 2010, 28 (50) 7897-7906 10.1016/j.vaccine.2010.09.077
13. García-Vallejo, J. J.; Ambrosini, M.; Overbeek, A.; van Riel, W. E.; Bloem, K.; Unger, W. W. J.; Chiodo, F.; Bolscher, J. G.; Nazmi, K.; Kalay, H.; van Kooyk, Y. Multivalent Glycopeptide Dendrimers for the Targeted Delivery of Antigens to Dendritic Cells Mol. Immunol. 2013, 53 (4) 387-397 10.1016/j.molimm.2012.09.012
14. Moffat, J. M.; Cheong, W. S.; Villadangos, J. A.; Mintern, J. D.; Netter, H. J. Hepatitis B Virus-like Particles access major Histocompatibility Class I and II Antigen Presentation Pathways in Primary Dendritic Cells Vaccine 2013, 31 (18) 2310-2316 10.1016/j.vaccine.2013.02.042
15. Unger, W. W. J.; Van Beelen, A. J.; Bruijns, S. C.; Joshi, M.; Fehres, C. M.; Van Bloois, L.; Verstege, M. I.; Ambrosini, M.; Kalay, H.; Nazmi, K.; Bolscher, J. G.; Hooijberg, E.; De Gruijl, T. D.; Storm, G.; Van Kooyk, Y. Glycan-modified Liposomes boost CD4 + and CD8 + T-cell Responses by Targeting DC-SIGN on Dendritic Cells J. Controlled Release 2012, 160 (1) 88-95 10.1016/j.jconrel.2012.02.007
16. Chiodo, F.; Marradi, M.; Park, J.; Ram, A. F. J.; Penadés, S.; Van Die, I.; Tefsen, B. Galactofuranose-coated Gold Nanoparticles elicit a Pro-inflammatory Response in Human Monocyte-derived Dendritic Cells and are recognized by DC-SIGN ACS Chem. Biol. 2014, 9 (2) 383-389 10.1021/cb4008265
17. Shahbazi, M. A.; Fernández, T. D.; Mäkilä, E. M.; Le Guével, X.; Mayorga, C.; Kaasalainen, M. H.; Salonen, J. J.; Hirvonen, J. T.; Santos, H. A. Surface Chemistry Dependent Immunostimulative Potential of Porous Silicon Nanoplatforms Biomaterials 2014, 35 (33) 9224-9235 10.1016/j.biomaterials.2014.07.050
18. Tomić, S.; Dokić, J.; Vasilijić, S.; Ogrinc, N.; Rudolf, R.; Pelicon, P.; Vučević, D.; Milosavljević, P.; Janković, S.; Anžel, I.; Rajković, J.; Rupnik, M. S.; Friedrich, B.; Čolić, M. Size-Dependent Effects of Gold Nanoparticles Uptake on Maturation and Antitumor Functions of Human Dendritic Cells In Vitro PLoS One 2014, 9 (5) e96584 10.1371/journal.pone.0096584
19. Reddy, S. T.; Van Der Vlies, A. J.; Simeoni, E.; Angeli, V.; Randolph, G. J.; O'Neil, C. P.; Lee, L. K.; Swartz, M. A.; Hubbell, J. A. Exploiting Lymphatic Transport and Complement Activation in Nanoparticle Vaccines Nat. Biotechnol. 2007, 25 (10) 1159-1164 10.1038/nbt1332
20. Huo, S.; Ma, H.; Huang, K.; Liu, J.; Wei, T.; Jin, S.; Zhang, J.; He, S.; Liang, X. J. Superior Penetration and Retention Behavior of 50 nm Gold Nanoparticles in Tumors Cancer Res. 2013, 73 (1) 319-330 10.1158/0008-5472.CAN-12-2071
21. Hirsjärvi, S.; Dufort, S.; Gravier, J.; Texier, I.; Yan, Q.; Bibette, J.; Sancey, L.; Josserand, V.; Passirani, C.; Benoit, J. P.; Coll, J. L. Influence of Size, Surface Coating and Fine Chemical Composition on the In Vitro Reactivity and In Vivo Biodistribution of Lipid Nanocapsules versus Lipid Nanoemulsions in Cancer Models Nanomedicine 2013, 9 (3) 375-387 10.1016/j.nano.2012.08.005
22. Moros, M.; Hernáez, B.; Garet, E.; Dias, J. T.; Sáez, B.; Grazú, V.; González-Fernández, A.; Alonso, C.; De La Fuente, J. M. Monosaccharides versus PEG-Functionalized NPs: Influence in the Cellular Uptake ACS Nano 2012, 6 (2) 1565-1577 10.1021/nn204543c
23. Figdor, C. G.; Van Kooyk, Y.; Adema, G. J. C-type Lectin Receptors on Dendritic Cells and Langerhans Cells Nat. Rev. Immunol. 2002, 2 (2) 77-84 10.1038/nri723
24. Bernardi, A.; Jiménez-Barbero, J.; Casnati, A.; De Castro, C.; Darbre, T.; Fieschi, F.; Finne, J.; Funken, H.; Jaeger, K. E.; Lahmann, M.; Lindhorst, T. K.; Marradi, M.; Messner, P.; Molinaro, A.; Murphy, P. V.; Nativi, C.; Oscarson, S.; Penadés, S.; Peri, F.; Pieters, R. J.; Renaudet, O.; Reymond, J. L.; Richichi, B.; Rojo, J.; Sansone, F.; Schäffer, C.; Turnbull, W. B.; Velasco-Torrijos, T.; Vidal, S.; Vincent, S.; Wennekes, T.; Zuilhof, H.; Imberty, A. Multivalent Glycoconjugates as Anti-pathogenic Agents Chem. Soc. Rev. 2013, 42 (11) 4709-4727 10.1039/C2CS35408J
25. Ribeiro-Viana, R.; García-Vallejo, J. J.; Collado, D.; Pérez-Inestrosa, E.; Bloem, K.; Van Kooyk, Y.; Rojo, J. BODIPY-labeled DC-SIGN-Targeting Glycodendrons efficiently Internalize and Route to Lysosomes in Human Dendritic Cells Biomacromolecules 2012, 13 (10) 3209-3219 10.1021/bm300998c
26. Luczkowiak, J.; Muñoz, A.; Sánchez-Navarro, M.; Ribeiro-Viana, R.; Ginieis, A.; Illescas, B. M.; Martín, N.; Delgado, R.; Rojo, J. Glycofullerenes Inhibit Viral Infection Biomacromolecules 2013, 14 (2) 431-437 10.1021/bm3016658
27. Sattin, S.; Daghetti, A.; Thépaut, M.; Berzi, A.; Sánchez-Navarro, M.; Tabarani, G.; Rojo, J.; Fieschi, F.; Clerici, M.; Bernardi, A. Inhibition of DC-SIGN-Mediated HIV Infection by a Linear Trimannoside mimic in a Tetravalent Presentation ACS Chem. Biol. 2010, 5 (3) 301-312 10.1021/cb900216e
28. Luczkowiak, J.; Sattin, S.; Sutkevičiute, I.; Reina, J. J.; Sánchez-Navarro, M.; Thépaut, M.; Martínez-Prats, L.; Daghetti, A.; Fieschi, F.; Delgado, R.; Bernardi, A.; Rojo, J. Pseudosaccharide Functionalized Dendrimers as Potent Inhibitors of DC-SIGN Dependent Ebola Pseudotyped Viral Infection Bioconjugate Chem. 2011, 22 (7) 1354-1365 10.1021/bc2000403
29. Ribeiro-Viana, R.; Sánchez-Navarro, M.; Luczkowiak, J.; Koeppe, J. R.; Delgado, R.; Rojo, J.; Davis, B. G. Virus-like Glycodendrinanoparticles Displaying Quasi-equivalent nested Polyvalency upon Glycoprotein Platforms Potently Block Viral Infection Nat. Commun. 2012, 3, 1303 10.1038/ncomms2302
30. Jin, R. Quantum sized, Thiolate-protected Gold Nanoclusters Nanoscale 2010, 2 (3) 343-362 10.1039/B9NR00160C
31. Zheng, J.; Zhou, C.; Yu, M.; Liu, J. Different Sized Luminescent Gold Nanoparticles Nanoscale 2012, 4 (14) 4073-4083 10.1039/c2nr31192e
32. Zheng, J.; Nicovich, P. R.; Dickson, R. M. Highly Fluorescent Noble-Metal Quantum Dots Annu. Rev. Phys. Chem. 2007, 58, 409-431 10.1146/annurev.physchem.58.032806.104546
33. Goswami, N.; Zheng, K.; Xie, J. Bio-NCs-the Marriage of Ultrasmall Metal Nanoclusters with Biomolecules Nanoscale 2014, 6 (22) 13328-13347 10.1039/C4NR04561K
34. Jiang, D. E. The Expanding Universe of Thiolated Gold Nanoclusters and Beyond Nanoscale 2013, 5 (16) 7149-7160 10.1039/c3nr34192e
35. Zhu, M.; Aikens, C. M.; Hollander, F. J.; Schatz, G. C.; Jin, R. Correlating the Crystal Structure of a Thiol-protected Au25 Cluster and Optical Properties J. Am. Chem. Soc. 2008, 130 (18) 5883-5885 10.1021/ja801173r
36. Le Guével, X.; Tagit, O.; Rodríguez, C. E.; Trouillet, V.; Pernia Leal, M.; Hildebrandt, N. Ligand Effect on the Size, Valence State and Red/near Infrared Photoluminescence of Bidentate Thiol Gold Nanoclusters Nanoscale 2014, 6 (14) 8091-8099 10.1039/c4nr01130a
37. Negishi, Y.; Nobusada, K.; Tsukuda, T. Glutathione-protected Gold Clusters Revisited: Bridging the Gap between Gold(I)-thiolate Complexes and Thiolate-protected Gold Nanocrystals J. Am. Chem. Soc. 2005, 127 (14) 5261-5270 10.1021/ja042218h
38. Wang, G.; Guo, R.; Kalyuzhny, G.; Choi, J. P.; Murray, R. W. NIR Luminescence Intensities increase Linearly with Proportion of Polar Thiolate Ligands in Protecting Monolayers of Au 38 and Au 140 Quantum Dots J. Phys. Chem. B 2006, 110 (41) 20282-20289 10.1021/jp0640528
39. Yu, Y.; Luo, Z.; Chevrier, D. M.; Leong, D. T.; Zhang, P.; Jiang, D. E.; Xie, J. Identification of a Highly Luminescent Au22(SG)18 Nanocluster J. Am. Chem. Soc. 2014, 136 (4) 1246-1249 10.1021/ja411643u
40. Aldeek, F.; Muhammed, M. A. H.; Palui, G.; Zhan, N.; Mattoussi, H. Growth of Highly Fluorescent Polyethylene glycol- and Zwitterion- Functionalized Gold Nanoclusters ACS Nano 2013, 7 (3) 2509-2521 10.1021/nn305856t
41. Le Guével, X.; Spies, C.; Daum, N.; Jung, G.; Schneider, M. Highly Fluorescent Silver Nanoclusters Stabilized by Glutathione: A Promising Fluorescent Label for Bioimaging Nano Res. 2012, 5 (6) 379-387 10.1007/s12274-012-0218-1
42. Muhammed, M. A. H.; Ramesh, S.; Sinha, S. S.; Pal, S. K.; Pradeep, T. Two Distinct Fluorescent Quantum Clusters of Gold Starting from Metallic Nanoparticles by pH-Dependent Ligand Etching Nano Res. 2008, 1, 333-340 10.1007/s12274-008-8035-2
43. Le Guével, X.; Hötzer, B.; Jung, G.; Hollemeyer, K.; Trouillet, V.; Schneider, M. Formation of Fluorescent Metal (Au, Ag) Nanoclusters Capped in Bovine Serum Albumin Followed by Fluorescence and Spectroscopy J. Phys. Chem. C 2011, 115 (22) 10955-10963 10.1021/jp111820b
44. Shang, L.; Azadfar, N.; Stockmar, F.; Send, W.; Trouillet, V.; Bruns, M.; Gerthsen, D.; Nienhaus, G. U. One-pot Synthesis of Near-infrared Fluorescent Gold Clusters for Cellular Fluorescence Lifetime Imaging Small 2011, 7 (18) 2614-2620 10.1002/smll.201100746
45. Luo, Z.; Yuan, X.; Yu, Y.; Zhang, Q.; Leong, D. T.; Lee, J. Y.; Xie, J. From Aggregation-induced Emission of Au(I)-thiolate Complexes to Ultrabright Au(0)@Au(I)-Thiolate Core-shell Nanoclusters J. Am. Chem. Soc. 2012, 134 (40) 16662-16670 10.1021/ja306199p
46. Chan, P. H.; Ghosh, B.; Lai, H. Z.; Peng, H. L.; Mong, K. K. T.; Chen, Y. C. Photoluminescent Gold Nanoclusters as Sensing Probes for Uropathogenic Escherichia coli PLoS One 2013, 8 (3) e58064 10.1371/journal.pone.0058064
47. Wang, H. H.; Lin, C. A. J.; Lee, C. H.; Lin, Y. C.; Tseng, Y. M.; Hsieh, C. L.; Chen, C. H.; Tsai, C. H.; Hsieh, C. T.; Shen, J. L.; Chan, W. H.; Chang, W. H.; Yeh, H. I. Fluorescent Gold Nanoclusters as a Biocompatible Marker for In Vitro and In Vivo Tracking of Endothelial Cells ACS Nano 2011, 5 (6) 4337-4344 10.1021/nn102752a
48. Kunwar, P.; Hassinen, J.; Bautista, G.; Ras, R. H. A.; Toivonen, J. Direct Laser Writing of Photostable Fluorescent Silver Nanoclusters in Polymer Films ACS Nano 2014, 8 (11) 11165-11171 10.1021/nn5059503
49. Liu, J.; Yu, M.; Zhou, C.; Yang, S.; Ning, X.; Zheng, J. Passive Tumor Targeting of Renal-Clearable Luminescent Gold Nanoparticles: Long Tumor Retention and Fast Normal Tissue Clearance J. Am. Chem. Soc. 2013, 135 (13) 4978-4981 10.1021/ja401612x
50. Zhou, C.; Long, M.; Qin, Y.; Sun, X.; Zheng, J. Luminescent Gold Nanoparticles with Efficient Renal Clearance Angew. Chem., Int. Ed. 2011, 50 (14) 3168-3172 10.1002/anie.201007321
51. Zhang, X. D.; Chen, J.; Luo, Z.; Wu, D.; Shen, X.; Song, S. S.; Sun, Y. M.; Liu, P. X.; Zhao, J.; Huo, S.; Fan, S.; Fan, F.; Liang, X. J.; Xie, J. Enhanced Tumor Accumulation of Sub-2 nm Gold Nanoclusters for Cancer Radiation Therapy Adv. Healthcare Mater. 2014, 3 (1) 133-141 10.1002/adhm.201300189
52. Fernandez, T. D.; Pearson, J. R.; Leal, M. P.; Torres, M. J.; Blanca, M.; Mayorga, C.; Le Guével, X. Intracellular Accumulation and Immunological Properties of Fluorescent Gold Nanoclusters in Human Dendritic Cells Biomaterials 2015, 43, 1-12 10.1016/j.biomaterials.2014.11.045
53. Park, J.; Nam, J.; Won, N.; Jin, H.; Jung, S.; Jung, S.; Cho, S. H.; Kim, S. Compact and Stable Quantum Dots with Positive, Negative, or Zwitterionic Surface: Specific Cell Interactions and Non-specific Adsorptions by the Surface Charges Adv. Funct. Mater. 2011, 21 (9) 1558-1566 10.1002/adfm.201001924
54. Dou, X.; Yuan, X.; Yao, Q.; Luo, Z.; Zheng, K.; Xie, J. Facile Synthesis of Water-soluble Au25-xAgx Nanoclusters protected by Mono- and Bi-thiolate ligands Chem. Commun. 2014, 50 (56) 7459-7462 10.1039/c4cc02261k
55. Wu, Z.; Jin, R. On the Ligands Role in the Fluorescence of Gold Nanoclusters Nano Lett. 2010, 10 (7) 2568-2573 10.1021/nl101225f
56. Le Guevel, X. Recent Advances on the Synthesis of Metal Quantum Nanoclusters and their Application for Bioimaging IEEE J. Sel. Top. Quantum Electron. 2014, 20 (3) 1-12 10.1109/JSTQE.2013.2282275
57. Zhou, C.; Sun, C.; Yu, M.; Qin, Y.; Wang, J.; Kim, M.; Zheng, J. Luminescent Gold Nanoparticles with Mixed Valence States Generated from Dissociation of Polymeric Au(I) Thiolates J. Phys. Chem. C 2010, 114 (17) 7727-7732 10.1021/jp9122584
58. Hong, Y.; Lam, J. W. Y.; Tang, B. Z. Aggregation-induced Emission Chem. Soc. Rev. 2011, 40 (11) 5361-5388 10.1039/c1cs15113d
59. Jia, X.; Li, J.; Wang, E. Cu Nanoclusters with Aggregation Induced Emission Enhancement Small 2013, 9 (22) 3873-3879 10.1002/smll.201300896
60. Dunn, K. W.; Kamocka, M. M.; McDonald, J. H. A Practical Guide to Evaluating Colocalization in Biological Microscopy American Journal of Physiology-Cell Physiology 2011, 300 (4) C723-C742 10.1152/ajpcell.00462.2010
61. Engering, A. J.; Cella, M.; Fluitsma, D.; Brockhaus, M.; Hoefsmit, E. C. M.; Lanzavecchia, A.; Pieters, J. The Mannose Receptor Functions as a High Capacity and Broad Specificity Antigen Receptor in Human Dendritic Cells Eur. J. Immunol. 1997, 27 (9) 2417-2425 10.1002/eji.1830270941
62. 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 J. Controlled Release 2009, 135 (3) 259-267 10.1016/j.jconrel.2009.01.018
63. Khalil, I. A.; Kogure, K.; Akita, H.; Harashima, H. Uptake Pathways and Subsequent Intracellular Trafficking in Nonviral Gene Delivery Pharmacol. Rev. 2006, 58 (1) 32-45 10.1124/pr.58.1.8
64. Chen, C. L.; Hou, W. H.; Liu, I. H.; Hsiao, G.; Huang, S. S.; Huang, J. S. Inhibitors of Clathrin-dependent Endocytosis enhance TGFβ Signaling and Responses J. Cell Sci. 2009, 122 (11) 1863-1871 10.1242/jcs.038729
65. Macia, E.; Ehrlich, M.; Massol, R.; Boucrot, E.; Brunner, C.; Kirchhausen, T. Dynasore, a Cell-Permeable Inhibitor of Dynamin Dev. Cell 2006, 10 (6) 839-850 10.1016/j.devcel.2006.04.002
66. Shang, L.; Nienhaus, K.; Jiang, X.; Yang, L.; Landfester, K.; Mailänder, V.; Simmet, T.; Nienhaus, G. Nanoparticle Interactions with Live Cells: Quantitative Fluorescence Microscopy of Nanoparticle Size Effects Beilstein J. Nanotechnol. 2014, 5, 2388-2397 10.3762/bjnano.5.248
67. Falcone, S.; Cocucci, E.; Podini, P.; Kirchhausen, T.; Clementi, E.; Meldolesi, J. Macropinocytosis: Regulated Coordination of Endocytic and Exocytic Membrane Traffic Events J. Cell Sci. 2006, 119 (22) 4758-4769 10.1242/jcs.03238
68. Zegers, M. M. P.; Zaal, K. J. M.; Van Ijzendoorn, S. C. D.; Klappe, K.; Hoekstra, D. Actin Filaments and Microtubules are Involved in Different Membrane Traffic Pathways that Transport Sphingolipids to the Apical Surface of Polarized HepG2 cells Mol. Biol. Cell 1998, 9 (7) 1939-1949 10.1091/mbc.9.7.1939
69. Zhang, L. W.; Bäumer, W.; Monteiro-Riviere, N. A. Cellular Uptake Mechanisms and Toxicity of Quantum Dots in Dendritic Cells Nanomedicine 2011, 6 (5) 777-791 10.2217/nnm.11.73
70. dos Santos, T.; Varela, J.; Lynch, I.; Salvati, A.; Dawson, K. A. Effects of Transport Inhibitors on the Cellular Uptake of Carboxylated Polystyrene Nanoparticles in Different Cell Lines PLoS One 2011, 6 (9) e24438 10.1371/journal.pone.0024438