Gold Nanoparticles Induced Endothelial Leakiness Depends on Particle Size and Endothelial Cell Origin

ACS Nano

Volumn 11, Issue 5, 2017, Pages 5020-5030

  Setyawati, Magdiel I ^a   Tay, Chor Yong ^b,c   Bay, Boon Huat ^a   Leong, David T ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

endothelial cell permeability; endothelial permeability and retention; gold; nanoparticle; nanoparticle induced endothelial leakiness

Indexed keywords

ACCESS CONTROL; BLOOD VESSELS; CELLS; CYTOLOGY; GOLD; MEDICAL NANOTECHNOLOGY; NANOPARTICLES; NANOTECHNOLOGY; PARTICLE SIZE; TUMORS;

CELL PERMEABILITY; CONTROL ACCESS; ENDOTHELIAL PERMEABILITY; GOLD NANOPARTICLES; HUMAN SKIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; SIDE EFFECT; TUMOR SITE;

ENDOTHELIAL CELLS;

GOLD; METAL NANOPARTICLE; NANOPARTICLE;

CHEMISTRY; DRUG EFFECT; ENDOTHELIUM; HUMAN; METABOLISM; NANOMEDICINE; PARTICLE SIZE; PERMEABILITY; PHYSIOLOGY; TUMOR CELL LINE; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

CELL LINE, TUMOR; ENDOTHELIUM; ENDOTHELIUM, VASCULAR; GOLD; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; METAL NANOPARTICLES; NANOMEDICINE; NANOPARTICLES; PARTICLE SIZE; PERMEABILITY;

EID: 85019918392     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.7b01744     Document Type: Article

References (44)

1. Dejana, E. Endothelial Cell-Cell Junctions: Happy Together Nat. Rev. Mol. Cell Biol. 2004, 5, 261-270 10.1038/nrm1357
2. Howard, M.; Zern, B. J.; Anselmo, A. C.; Shuvaev, V. V.; Mitragotri, S.; Muzykantov, V. Vascular Targeting of Nanocarriers: Perplexing Aspects of the Seemingly Straightforward Paradigm ACS Nano 2014, 8, 4100-4132 10.1021/nn500136z
3. von Roemeling, C.; Jiang, W.; Chan, C. K.; Weissman, I. L.; Kim, B. Y. Breaking Down the Barriers to Precision Cancer Nanomedicine Trends Biotechnol. 2016, 35, 159-171 10.1016/j.tibtech.2016.07.006
4. Setyawati, M. I.; Tay, C. Y.; Docter, D.; Stauber, R. H.; Leong, D. T. Understanding and Exploiting Nanoparticles' Intimacy with the Blood Vessel and Blood Chem. Soc. Rev. 2015, 44, 8174-8199 10.1039/C5CS00499C
5. Bae, Y. H.; Park, K. Targeted Drug Delivery to Tumors: Myths, Reality and Possibility J. Controlled Release 2011, 153, 198-205 10.1016/j.jconrel.2011.06.001
6. Cao, J.; Wang, R.; Gao, N.; Li, M.; Tian, X.; Yang, W.; Ruan, Y.; Zhou, C.; Wang, G.; Liu, X.; Tang, S.; Yu, Y.; Liu, Y.; Sun, G.; Peng, H.; Wang, Q. A7RC Peptide Modified Paclitaxel Liposomes Dually Target Breast Cancer Biomater. Sci. 2015, 3, 1545-1554 10.1039/C5BM00161G
7. Wang, Q.; Cheng, H.; Peng, H.; Zhou, H.; Li, P. Y.; Langer, R. Non-Genetic Engineering of Cells for Drug Delivery and Cell-Based Therapy Adv. Drug Delivery Rev. 2015, 91, 125-140 10.1016/j.addr.2014.12.003
8. Jain, R. K.; Stylianopoulos, T. Delivering Nanomedicine to Solid Tumors Nat. Rev. Clin. Oncol. 2010, 7, 653-664 10.1038/nrclinonc.2010.139
9. Kutty, R. V.; Chia, S. L.; Setyawati, M. I.; Muthu, M. S.; Feng, S.-S.; Leong, D. T. In vivo and Ex vivo Proofs of Concept that Cetuximab Conjugated Vitamin E TPGS Micelles Increases Efficacy of Delivered Docetaxel against Triple Negative Breast Cancer Biomaterials 2015, 63, 58-69 10.1016/j.biomaterials.2015.06.005
10. Du, D.; Chang, N.; Sun, S.; Li, M.; Yu, H.; Liu, M.; Liu, X.; Wang, G.; Li, H.; Liu, X.; Geng, S.; Wang, Q.; Peng, H. The Role of Glucose Transporters in the Distribution of p-aminophenyl-alpha-D-mannopyranoside Modified Liposomes within Mice Brain J. Controlled Release 2014, 182, 99-110 10.1016/j.jconrel.2014.03.006
11. Kennedy, I. M.; Wilson, D.; Barakat, A. I. Uptake and Inflammatory Effects of Nanoparticles in a Human Vascular Endothelial Cell Line Res. Rep.-Health Eff. Inst. 2009, 136, 3-32
12. Khanna, P.; Ong, C.; Bay, B.; Baeg, G. Nanotoxicity: An Interplay of Oxidative Stress, Inflammation and Cell Death Nanomaterials 2015, 5, 1163 10.3390/nano5031163
13. Liu, X.; Sun, J. Endothelial Cells Dysfunction Induced by Silica Nanoparticles Through Oxidative Stress via JNK/P53 and NF-κB Pathways Biomaterials 2010, 31, 8198-8209 10.1016/j.biomaterials.2010.07.069
14. Bazzoni, G.; Dejana, E. Endothelial Cell-to-Cell Junctions: Molecular Organization and Role in Vascular Homeostasis Physiol. Rev. 2004, 84, 869-901 10.1152/physrev.00035.2003
15. Tay, C. Y.; Setyawati, M. I.; Leong, D. T. Nanoparticle Density: A Critical Biophysical Regulator of Endothelial Permeability ACS Nano 2017, 11, 2764-2772 10.1021/acsnano.6b07806
16. Setyawati, M. I.; Mochalin, V. N.; Leong, D. T. Tuning Endothelial Permeability with Functionalized Nanodiamonds ACS Nano 2016, 10, 1170-1181 10.1021/acsnano.5b06487
17. Setyawati, M. I.; Tay, C. Y.; Chia, S. L.; Goh, S. L.; Fang, W.; Neo, M. J.; Chong, H. C.; Tan, S. M.; Loo, S. C.; Ng, K. W.; Xie, J. P.; Ong, C. N.; Tan, N. S.; Leong, D. T. Titanium Dioxide Nanomaterials Cause Endothelial Cell Leakiness by Disrupting the Homophilic Interaction of VE-cadherin Nat. Commun. 2013, 4, 1673 10.1038/ncomms2655
18. Oda, H.; Takeichi, M. Evolution: Structural and Functional Diversity of Cadherin at the Adherens Junction J. Cell Biol. 2011, 193, 1137-1146 10.1083/jcb.201008173
19. Satchell, S. C.; Braet, F. Glomerular Endothelial Cell Fenestrations: An Integral Component of the Glomerular Filtration Barrier Am. J. Physiol. Renal Physiol. 2009, 296, F947-956 10.1152/ajprenal.90601.2008
20. Taveau, J. C.; Dubois, M.; Le Bihan, O.; Trepout, S.; Almagro, S.; Hewat, E.; Durmort, C.; Heyraud, S.; Gulino-Debrac, D.; Lambert, O. Structure of Artificial and Natural VE-cadherin-Based Adherens Junctions Biochem. Soc. Trans. 2008, 36, 189-193 10.1042/BST0360189
21. Yuan, S. Y.; Rigor, R. R. The Endothelial Barrier. In Regulation of Endothelial Barrier Function; Granger, D. N.; Granger, J. P., Eds.; Morgan & Claypool: San Rafael, 2010; http://www.ncbi.nlm.nih.gov/books/NBK54123/.
22. Boisselier, E.; Astruc, D. Gold Nanoparticles in Nanomedicine: Preparations, Imaging, Diagnostics, Therapies and Toxicity Chem. Soc. Rev. 2009, 38, 1759-1782 10.1039/b806051g
23. Peng, H.; Wang, C.; Xu, X.; Yu, C.; Wang, Q. An Intestinal Trojan Horse for Gene Delivery Nanoscale 2015, 7, 4354-4360 10.1039/C4NR06377E
24. 10-12 Nanomolecules for High Tumor Specificity and Cancer Radiotherapy Adv. Mater. 2014, 26, 4565-4568 10.1002/adma.201400866
25. Zhang, X.-D.; Luo, Z.; Chen, J.; Wang, H.; Song, S.-S.; Shen, X.; Long, W.; Sun, Y.-M.; Fan, S.; Zheng, K.; Leong, D. T.; Xie, J. Storage of Gold Nanoclusters in Muscle Leads to Their Biphasic In vivo Clearance Small 2015, 11, 1683-1690 10.1002/smll.201402233
26. Bastús, N. G.; Comenge, J.; Puntes, V. Kinetically Controlled Seeded Growth Synthesis of Citrate-Stabilized Gold Nanoparticles of up to 200 nm: Size Focusing versus Ostwald Ripening Langmuir 2011, 27, 11098-11105 10.1021/la201938u
27. Apopa, P. L.; Qian, Y.; Shao, R.; Guo, N. L.; Schwegler-Berry, D.; Pacurari, M.; Porter, D.; Shi, X.; Vallyathan, V.; Castranova, V.; Flynn, D. C. Iron Oxide Nanoparticles Induce Human Microvascular Endothelial Cell Permeability Through Reactive Oxygen Species Production and Microtubule Remodeling Part. Fibre Toxicol. 2009, 6, 1 10.1186/1743-8977-6-1
28. 2 Nanoparticles Biomaterials 2012, 33, 886-896 10.1016/j.biomaterials.2011.10.025
29. Pober, J. S.; Sessa, W. C. Evolving Functions of Endothelial Cells in Inflammation Nat. Rev. Immunol. 2007, 7, 803-815 10.1038/nri2171
30. Kempe, S.; Kestler, H.; Lasar, A.; Wirth, T. NF-κB Controls the Global Pro-Inflammatory Response in Endothelial Cells: Evidence for the Regulation of a Pro-Atherogenic Program Nucleic Acids Res. 2005, 33, 5308-5319 10.1093/nar/gki836
31. Zhang, X. D.; Luo, Z.; Chen, J.; Song, S.; Yuan, X.; Shen, X.; Wang, H.; Sun, Y.; Gao, K.; Zhang, L.; Fan, S.; Leong, D. T.; Guo, M.; Xie, J. Ultrasmall Glutathione-Protected Gold Nanoclusters as Next Generation Radiotherapy Sensitizers with High Tumor Uptake and High Renal Clearance Sci. Rep. 2015, 5, 8669 10.1038/srep08669
32. Shukla, R.; Bansal, V.; Chaudhary, M.; Basu, A.; Bhonde, R. R.; Sastry, M. Biocompatibility of Gold Nanoparticles and Their Endocytotic Fate Inside the Cellular Compartment: A Microscopic Overview Langmuir 2005, 21, 10644-10654 10.1021/la0513712
33. Tay, C. Y.; Setyawati, M. I.; Xie, J.; Parak, W. J.; Leong, D. T. Back to Basics: Exploiting the Innate Physico-chemical Characteristics of Nanomaterials for Biomedical Applications Adv. Funct. Mater. 2014, 24, 5936-5955 10.1002/adfm.201401664
34. Chithrani, B. D.; Ghazani, A. A.; Chan, W. C. Determining the Size and Shape Dependence of Gold Nanoparticle Uptake into Mammalian Cells Nano Lett. 2006, 6, 662-668 10.1021/nl052396o
35. Nel, A. E.; Madler, L.; Velegol, D.; Xia, T.; Hoek, E. M. V.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557 10.1038/nmat2442
36. Zarska, M.; Novotny, F.; Havel, F.; Sramek, M.; Babelova, A.; Benada, O.; Novotny, M.; Saran, H.; Kuca, K.; Musilek, K.; Hvezdova, Z.; Dzijak, R.; Vancurova, M.; Krejcikova, K.; Gabajova, B.; Hanzlikova, H.; Kyjacova, L.; Bartek, J.; Proska, J.; Hodny, Z. Two-Step Mechanism of Cellular Uptake of Cationic Gold Nanoparticles Modified by (16-Mercaptohexadecyl)trimethylammonium Bromide Bioconjugate Chem. 2016, 27, 2558-2574 10.1021/acs.bioconjchem.6b00491
37. Mehta, D.; Malik, A. B. Signaling Mechanisms Regulating Endothelial Permeability Physiol. Rev. 2006, 86, 279-367 10.1152/physrev.00012.2005
38. Birukova, A. A.; Tian, Y.; Dubrovskyi, O.; Zebda, N.; Sarich, N.; Tian, X.; Wang, Y.; Birukov, K. G. VE-cadherin Trans-Interactions Modulate Rac Activation and Enhancement of Lung Endothelial Barrier by Iloprost J. Cell. Physiol. 2012, 227, 3405-3416 10.1002/jcp.24041
39. Huang, R. L.; Teo, Z.; Chong, H. C.; Zhu, P.; Tan, M. J.; Tan, C. K.; Lam, C. R.; Sng, M. K.; Leong, D. T.; Tan, S. M.; Kersten, S.; Ding, J. L.; Li, H. Y.; Tan, N. S. ANGPTL4 Modulates Vascular Junction Integrity by Integrin Signaling and Disruption of Intercellular VE-cadherin and Claudin-5 Clusters Blood 2011, 118, 3990-4002 10.1182/blood-2011-01-328716
40. Adam, A. P.; Sharenko, A. L.; Pumiglia, K.; Vincent, P. A. Src-induced Tyrosine Phosphorylation of VE-cadherin Is Not Sufficient to Decrease Barrier Function of Endothelial Monolayers J. Biol. Chem. 2010, 285, 7045-7055 10.1074/jbc.M109.079277
41. Hatanaka, K.; Simons, M.; Murakami, M. Phosphorylation of VE-cadherin Controls Endothelial Phenotypes via p120-Catenin Coupling and Rac1 Activation Am. J. Physiol.: Heart Circ. Physiol. 2011, 300, H162-H172 10.1152/ajpheart.00650.2010
42. Maekawa, M.; Ishizaki, T.; Boku, S.; Watanabe, N.; Fujita, A.; Iwamatsu, A.; Obinata, T.; Ohashi, K.; Mizuno, K.; Narumiya, S. Signaling from Rho to the Actin Cytoskeleton through Protein Kinases ROCK and LIM-Kinase Science 1999, 285, 895-898 10.1126/science.285.5429.895
43. Kaunas, R.; Nguyen, P.; Usami, S.; Chien, S. Cooperative Effects of Rho and Mechanical Stretch on Stress Fiber Organization Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 15895-15900 10.1073/pnas.0506041102
44. Rüffer, C.; Strey, A.; Janning, A.; Kim, K. S.; Gerke, V. Cell-Cell Junctions of Dermal Microvascular Endothelial Cells Contain Tight and Adherens Junction Proteins in Spatial Proximity Biochemistry 2004, 43, 5360-5369 10.1021/bi035517c