627
Views
38
CrossRef citations to date
0
Altmetric
Articles

Angiopoietin-1 accelerates restoration of endothelial cell barrier integrity from nanoparticle-induced leakiness

, , , &
Pages 682-700 | Received 04 Sep 2018, Accepted 14 Jan 2019, Published online: 19 Feb 2019

References

  • Apopa, P. L., Y. Qian, R. Shao, N. L. Guo, D. Schwegler-Berry, M. Pacurari, D. Porter, et al. 2009. “Iron Oxide Nanoparticles Induce Human Microvascular Endothelial Cell Permeability through Reactive Oxygen Species Production and Microtubule Remodeling.” Particle and Fibre Toxicology 6: 1. doi:10.1186/1743-8977-6-1
  • Astanina, K., Y. Simon, C. Cavelius, S. Petry, A. Kraegeloh, and A. K. Kiemer. 2014. “Superparamagnetic Iron Oxide Nanoparticles Impair Endothelial Integrity and Inhibit Nitric Oxide Production.” Acta Biomaterialia 10 (11):4896–4911. doi:10.1016/j.actbio.2014.07.027
  • Balaji, S., N. Han, C. Moles, A. F. Shaaban, P. L. Bollyky, T. M. Crombleholme, and S. G. Keswani. 2015. “Angiopoietin-1 Improves Endothelial Progenitor Cell-dependent Neovascularization in Diabetic Wounds.” Surgery 158 (3): 846–856. doi:10.1016/j.surg.2015.06.034
  • Bergmeier, W., and R. O. Hynes. 2012. “Extracellular Matrix Proteins in Hemostasis and Thrombosis.” Cold Spring Harbor.” Perspectives in Biology 4 (2): a005132. doi:10.1101/cshperspect.a005132.
  • Bogdanovic, E., V. P. Nguyen, and D. J. Dumont. 2006. “Activation of Tie2 by Angiopoietin-1 and Angiopoietin-2 Results in Their Release and Receptor Internalization.” Journal of Cell Science 119 (Pt 17): 3551–3560. doi:10.1242/jcs.03077
  • Cantelmo, A. R., L.-C. Conradi, A. Brajic, J. Goveia, J. Kalucka, A. Pircher, P. Chaturvedi, et al. 2016. “Inhibition of the Glycolytic Activator PFKFB3 in Endothelium Induces Tumor Vessel Normalization, Impairs Metastasis, and Improves Chemotherapy.” Cancer Cell 30 (6): 968–985. doi:10.1016/j.ccell.2016.10.006
  • Dai, Y., C. Xu, X. Sun, and X. Chen. 2017. “Nanoparticle Design Strategies for Enhanced Anticancer Therapy by Exploiting the Tumour Microenvironment.” Chemical Society Reviews 46 (12): 3830–3852. doi:10.1039/C6CS00592F
  • Danielsen, P. H., Y. Cao, M. Roursgaard, P. Møller, and S. Loft. 2015. “Endothelial Cell Activation, Oxidative Stress and Inflammation Induced by a Panel of Metal-Based Nanomaterials.” Nanotoxicology 9 (7): 813–824. doi:10.3109/17435390.2014.980449
  • Dewhirst, M. W., and T. W. Secomb. 2017. “Transport of Drugs from Blood Vessels to Tumour Tissue.” Nature Reviews Cancer 17 (12): 738. doi:10.1038/nrc.2017.93
  • Drees, F., S. Pokutta, S. Yamada, W. J. Nelson, and W. I. Weis. 2005. “Alpha-catenin is a Molecular Switch that Binds E-Cadherin-Beta-Catenin and Regulates Actin-filament assembly.” Cell 123 (5): 903–915. doi:10.1016/j.cell.2005.09.021
  • Frye, M., M. Dierkes, V. Küppers, M. Vockel, J. Tomm, D. Zeuschner, J. Rossaint, et al. 2015. “Interfering with VE-PTP Stabilizes Endothelial Junctions in Vivo via Tie-2 in the Absence of VE-Cadherin.” The Journal of Experimental Medicine 212 (13): 2267–2287. doi:10.1084/jem.20150718
  • Fukuhara, S., K. Sako, T. Minami, K. Noda, H. Z. Kim, T. Kodama, M. Shibuya, N. Takakura, G. Y. Koh, and N. Mochizuki. 2008. “Differential Function of Tie2 at cell-cell contacts and cell-substratum Contacts Regulated by Angiopoietin-1.” Nature Cell Biology 10 (5): 513. doi:10.1038/ncb1714
  • Fukuhara, S., K. Sako, K. Noda, K. Nagao, K. Miura, and N. Mochizuki. 2009. “Tie2 Is Tied at the Cell-Cell Contacts and to Extracellular Matrix by angiopoietin-1.” Experimental & Molecular Medicine 41 (3): 133. doi:10.3858/emm.2009.41.3.016
  • Fuxe, J., S. Tabruyn, K. Colton, H. Zaid, A. Adams, P. Baluk, E. Lashnits, et al. 2011. “Pericyte Requirement for Anti-leak Action of Angiopoietin-1 and Vascular Remodeling in Sustained Inflammation.” The American Journal of Pathology 178 (6): 2897–2909. doi:10.1016/j.ajpath.2011.02.008.
  • Galie, P. A., D.-H. T. Nguyen, C. K. Choi, D. M. Cohen, P. A. Janmey, and C. S. Chen. 2014. “Fluid Shear Stress Threshold Regulates Angiogenic Sprouting.” Proceedings of the National Academy of Sciences 111 (22): 7968–7973. doi:10.1073/pnas.1310842111.
  • Gamble, J. R., J. Drew, L. Trezise, A. Underwood, M. Parsons, L. Kasminkas, J. Rudge, G. Yancopoulos, and M. A. Vadas. 2000. “Angiopoietin-1 is an anti-Permeability and anti-Inflammatory Agent in Vitro and Targets Cell Junctions.” Circulation Research 87 (7): 603–607. doi:10.1161/01.RES.87.7.603.
  • Gavard, J., V. Patel, and J. S. Gutkind. 2008. “Angiopoietin-1 Prevents VEGF-Induced Endothelial Permeability by Sequestering Src through mDia.” Developmental Cell 14 (1): 25–36. doi:10.1016/j.devcel.2007.10.019
  • Ghosh, C. C., S. David, R. Zhang, A. Berghelli, K. Milam, S. J. Higgins, J. Hunter, et al. 2016. “Gene Control of Tyrosine Kinase TIE2 and Vascular Manifestations of Infections.” Proceedings of the National Academy of Sciences 113 (9): 2472–2477. doi:10.1073/pnas.1519467113.
  • Giannotta, M., M. Trani, and E. Dejana. 2013. “VE-Cadherin and Endothelial Adherens Junctions: Active Guardians of Vascular Integrity.” Developmental Cell 26 (5): 441–454. doi:10.1016/j.devcel.2013.08.020
  • Giner-Casares, J. J., M. Henriksen-Lacey, M. Coronado-Puchau, and L. M. Liz-Marzán. 2016. “Inorganic Nanoparticles for Biomedicine: Where Materials Scientists Meet Medical Research.” Materials Today 19 (1): 19–28. doi:10.1016/j.mattod.2015.07.004.
  • Hakanpaa, L., T. Sipila, V.-M. Leppanen, P. Gautam, H. Nurmi, G. Jacquemet, L. Eklund, J. Ivaska, K. Alitalo, and P. Saharinen. 2015. “Endothelial Destabilization by Angiopoietin-2 via Integrin β1 Activation.” Nature Communications 6: 5962. doi:10.1038/ncomms6962
  • Handa, T., T. Hirai, N. Izumi, S. I. Eto, S. I. Tsunoda, K. Nagano, K. Higashisaka, Y. Yoshioka, and Y. Tsutsumi. 2017. “Identifying a Size-specific Hazard of Silica Nanoparticles after Intravenous Administration and its Relationship to the Other Hazards that have Negative Correlations with the Particle Size in mice.” Nanotechnology 28 (13): 135101. doi:10.1088/1361-6528/aa5d7c
  • Hashizume, H., P. Baluk, S. Morikawa, J. W. McLean, G. Thurston, S. Roberge, R. K. Jain, and D. M. McDonald. 2000. “Openings between Defective Endothelial Cells Explain Tumor Vessel Leakiness.” The American Journal of Pathology 156 (4): 1363–1380. doi:10.1016/S0002-9440(10)65006-7
  • Ho, D. N., N. Kohler, A. Sigdel, R. Kalluri, J. R. Morgan, C. Xu, and S. Sun. 2012. “Penetration of Endothelial Cell Coated Multicellular Tumor Spheroids by Iron Oxide Nanoparticles.” Theranostics 2 (1): 66–75. doi:10.7150/thno.3568
  • Huynh, E., and G. Zheng. 2015. “Cancer Nanomedicine: Addressing the Dark Side of the Enhanced Permeability and Retention Effect.” Nanomedicine (London, England) 10 (13): 1993–1995. doi:10.2217/nnm.15.86.
  • Jain, R. K., and L. L. Munn. 2000. “Leaky Vessels? Call Ang1!” Nature Medicine 6 (2): 131. doi:10.1038/72212
  • Jiang, H., F. Zhang, J. Yang, and S. Han. 2014. “Angiopoietin-1 Ameliorates Inflammation-induced Vascular Leakage and Improves Functional Impairment in a Rat Model of Acute Experimental Autoimmune Encephalomyelitis.” Experimental Neurology 261: 245–257. doi:10.1016/j.expneurol.2014.05.013.
  • Jo, D. H., J. H. Kim, J. G. Son, N. W. Song, Y.-I. Kim, Y. S. Yu, T. G. Lee, and J. H. Kim. 2014. “Anti-angiogenic Effect of Bare Titanium Dioxide Nanoparticles on Pathologic Neovascularization without Unbearable Toxicity.” Nanomedicine: Nanotechnology, Biology and Medicine 10 (5): 1109–1117.
  • Korhonen, E. A., A. Lampinen, H. Giri, A. Anisimov, M. Kim, B. Allen, S. Fang, et al. 2016. “Tie1 Controls Angiopoietin Function in Vascular Remodeling and Inflammation.” Journal of Clinical Investigation 126 (9): 3495–3510. doi:10.1172/JCI84923.
  • Li, X., N. Padhan, E. O. Sjöström, F. P. Roche, C. Testini, N. Honkura, M. Sáinz-Jaspeado, et al. 2016. “VEGFR2 pY949 Signalling Regulates Adherens Junction Integrity and Metastatic Spread.” Nature Communications 7: 11017 doi:10.1038/ncomms11017
  • Lim, R. G., C. Quan, A. M. Reyes-Ortiz, S. E. Lutz, A. J. Kedaigle, T. A. Gipson, J. Wu, et al. 2017. “Huntington's Disease iPSC-derived Brain Microvascular Endothelial Cells Reveal WNT-mediated Angiogenic and Blood-Brain Barrier Deficits.” Cell Reports 19 (7): 1365–1377. doi:10.1016/j.celrep.2017.04.021.
  • Matsumoto, Y., J. W. Nichols, K. Toh, T. Nomoto, H. Cabral, Y. Miura, R. J. Christie, et al. 2016. “Vascular Bursts Enhance Permeability of Tumour Blood Vessels and Improve Nanoparticle Delivery.” Nature Nanotechnology 11 (6): 533. doi:10.1038/nnano.2015.342
  • McCarthy, N. 2012. “Leaky Effect.” Nature Reviews. Cancer 12 (3): 157. doi:10.1038/nrc3227
  • Michael, I. P., M. Orebrand, M. Lima, B. Pereira, O. Volpert, S. E. Quaggin, and M. Jeansson. 2017. “Angiopoietin-1 Deficiency Increases Tumor Metastasis in Mice.” BMC Cancer 17 (1): 539. doi:10.1186/s12885-017-3531-y
  • Mitragotri, S., D. G. Anderson, X. Chen, E. K. Chow, D. Ho, A. V. Kabanov, J. M. Karp, et al. 2015. “Accelerating the Translation of Nanomaterials in Biomedicine.” ACS Nano 9 (7): 6644–6654. doi:10.1021/acsnano.5b03569
  • Mundi, S., M. Massaro, E. Scoditti, M. A. Carluccio, V. W. M. van Hinsbergh, M. L. Iruela-Arispe, and R. De Caterina. 2018. “Endothelial Permeability, LDL Deposition, and Cardiovascular Risk Factors—a Review.” Cardiovascular Research 114 (1): 35–52. doi:10.1093/cvr/cvx226.
  • Nakamura, Y., A. Mochida, P. L. Choyke, and H. Kobayashi. 2016. “Nanodrug Delivery: Is the Enhanced Permeability and Retention Effect Sufficient for Curing Cancer?” Bioconjugate Chemistry 27 (10): 2225–2238. doi:10.1021/acs.bioconjchem.6b00437
  • Orsenigo, F., C. Giampietro, A. Ferrari, M. Corada, A. Galaup, S. Sigismund, G. Ristagno, et al. 2012. “Phosphorylation of VE-Cadherin is Modulated by Haemodynamic Forces and Contributes to the Regulation of Vascular Permeability in vivo.” Nature Communications 3: 1208. doi:10.1038/ncomms2199
  • Park-Windhol, C., and P. A. D'Amore. 2016. “Disorders of Vascular Permeability.” Annual Review of Pathology 11: 251–281. doi:10.1146/annurev-pathol-012615-044506
  • Peng, F., J. K. Tee, M. I. Setyawati, X. Ding, H. L. A. Yeo, Y. L. Tan, D. T. Leong, and H. K. Ho. 2018. “Inorganic Nanomaterials as Highly Efficient Inhibitors of Cellular Hepatic Fibrosis.” ACS Applied Materials & Interfaces 10 (38): 31938–31946. doi:10.1021/acsami.8b10527
  • Peng, F., M. I. Setyawati, J. K. Tee, X. Ding, J. Wang, M. E. Nga, H. K. Ho, and D. T. Leong. 2019. “Nanoparticles Promote in Vivo Breast Cancer Cells Intravasation and Extravasation by Inducing Endothelial Leakiness.” Nature Nanotechnology. (in press). doi:10.1038/s41565-018-0356-z.
  • Peng, F., M. I. Setyawati , J. K. Tee , X. Ding , J. Wang , M. E. Nga , H. K. Ho , and D. T. Leong. 2019. “Nanoparticles Promote in Vivo Breast Cancer Cells Intravasation and Extravasation by Inducing Endothelial Leakiness.” Nature Nanotechnology. doi:10.1038/s41565-018-0356-z.
  • Portran, D., L. Schaedel, Z. Xu, M. Thery, and M. V. Nachury. 2017. “Tubulin Acetylation Protects Long-Lived Microtubules against Mechanical Ageing.” Nature Cell Biology 19 (4): 391–398. doi:10.1038/ncb3481.
  • Qiu, Y., S. Tong, L. Zhang, Y. Sakurai, D. R. Myers, L. Hong, W. A. Lam, and G. Bao. 2017. “Magnetic Forces Enable Controlled Drug Delivery by Disrupting Endothelial Cell-Cell Junctions.” Nature Communications 8: 15594. doi:10.1038/ncomms15594
  • Saharinen, P., L. Eklund, and K. Alitalo. 2017. “Therapeutic Targeting of the Angiopoietin-TIE Pathway.” Nature Reviews. Drug Discovery 16 (9): 635. doi:10.1038/nrd.2016.278
  • Saharinen, P., L. Eklund, J. Miettinen, R. Wirkkala, A. Anisimov, M. Winderlich, A. Nottebaum, et al. 2008. “Angiopoietins Assemble Distinct Tie2 Signalling Complexes in Endothelial Cell-Cell and Cell-Matrix Contacts.” Nature Cell Biology 10 (5): 527–537. doi:10.1038/ncb1715
  • Schwartz, M. A., D. Vestweber, and M. Simons. 2018. “A Unifying Concept in Vascular Health and Disease.” Science (New York, N.Y.) 360 (6386): 270–271. doi:10.1126/science.aat3470
  • Setyawati, M. I., V. N. Mochalin, and D. T. Leong. 2016. “Tuning Endothelial Permeability with Functionalized Nanodiamonds.” ACS Nano 10 (1): 1170–1181. doi:10.1021/acsnano.5b06487
  • Setyawati, M. I., C. Y. Tay, B. H. Bay, and D. T. Leong. 2017. “Gold Nanoparticles Induced Endothelial Leakiness Depends on Particle Size and Endothelial Cell Origin.” ACS Nano 11 (5): 5020–5030. doi:10.1021/acsnano.7b01744
  • Setyawati, M. I., C. Y. Tay, S. L. Chia, S. L. Goh, W. Fang, M. J. Neo, H. C. Chong, et al. 2013. “Titanium Dioxide Nanomaterials Cause Endothelial Cell Leakiness by Disrupting the Homophilic Interaction of VE–Cadherin.” Nature Communications 4: 1673. doi:10.1038/ncomms2655
  • Setyawati, M. I., C. Y. Tay, D. Docter, R. H. Stauber, and D. T. Leong. 2015. “Understanding and Exploiting Nanoparticles' Intimacy with the Blood Vessel and Blood.” Chemical Society Reviews 44 (22): 8174–8199. doi:10.1039/C5CS00499C
  • Setyawati, M. I., C. Y. Tay, and D. T. Leong. 2014. “The Gap between Endothelial Cells: Key to the Quick Escape of Nanomaterials?” Nanomedicine (London, England) 9 (11): 1591–1514. doi:10.2217/nnm.14.104
  • Shi, J., P. W. Kantoff, R. Wooster, and O. C. Farokhzad. 2017. “Cancer Nanomedicine: Progress, Challenges and Opportunities.” Nature Reviews. Cancer 17 (1): 20–37. doi:10.1038/nrc.2016.108
  • Singh, S., S. R. Manson, H. Lee, Y. Kim, T. Liu, Q. Guo, J. J. Geminiani, P. F. Austin, and Y. M. Chen. 2016. “Tubular Overexpression of Angiopoietin-1 Attenuates Renal Fibrosis.” PloS One 11 (7): e0158908. doi:10.1371/journal.pone.0158908
  • Sukriti, S., M. Tauseef, P. Yazbeck, and D. Mehta. 2014. “Mechanisms Regulating Endothelial Permeability.” Pulmonary Circulation 4 (4): 535–551. doi:10.1086/677356
  • Tarbell, J. M. 2010. “Shear Stress and the Endothelial Transport Barrier.” Cardiovascular Research 87 (2): 320–330. doi:10.1093/cvr/cvq146
  • Tay, C. Y., M. I. Setyawati, and D. T. Leong. 2017. “Nanoparticle Density: A Critical Biophysical Regulator of Endothelial Permeability.” ACS Nano 11 (3): 2764–2772. doi:10.1021/acsnano.6b07806
  • Thurston, G., J. S. Rudge, E. Ioffe, H. Zhou, L. Ross, S. D. Croll, N. Glazer, J. Holash, D. M. McDonald, and G. D. Yancopoulos. 2000. “Angiopoietin-1 Protects the Adult Vasculature against Plasma Leakage.” Nature Medicine 6 (4): 460. doi:10.1038/74725
  • Viallard, C., and B. Larrivée. 2017. “Tumor Angiogenesis and Vascular Normalization: Alternative Therapeutic Targets.” Angiogenesis 20 (4): 409–426. doi:10.1007/s10456-017-9562-9
  • Wang, J., L. Zhang, F. Peng, X. Shi, and D. T. Leong. 2018. “Targeting Endothelial Cell Junctions with Negatively Charged Gold Nanoparticles.” Chemistry of Materials 30 (11): 3759–3767. doi:10.1021/acs.chemmater.8b00840.
  • Wu, F. T. H., C. R. Lee, E. Bogdanovic, A. Prodeus, J. Gariépy, and R. S. Kerbel. 2015. “Vasculotide Reduces Endothelial Permeability and Tumor Cell Extravasation in the Absence of Binding to or Agonistic Activation of Tie2.” EMBO Molecular Medicine 7 (6): 770–787. doi:10.15252/emmm.201404193.
  • Wu, Z., H. Yang, G. Archana, M. Rakshit, K. W. Ng, and C. Y. Tay. 2018. “Human Keratinocytes Adapt to ZnO Nanoparticles Induced Toxicity via Complex Paracrine Crosstalk and Nrf2-Proteasomal Signal Transduction.” Nanotoxicology 1–15. doi:10.1080/17435390.2018.1537409.
  • Xu, Z., L. Schaedel, D. Portran, A. Aguilar, J. Gaillard, M. P. Marinkovich, M. Théry, and M. V. Nachury. 2017. “Microtubules Acquire Resistance from Mechanical Breakage through Intralumenal Acetylation.” Science (New York, N.Y.) 356 (6335): 328–332. doi:10.1126/science.aai8764
  • Zhen, Z., W. Tang, Y. J. Chuang, T. Todd, W. Zhang, X. Lin, G. Niu, et al. 2014. “Tumor Vasculature Targeted Photodynamic Therapy for Enhanced Delivery of Nanoparticles.” ACS Nano 8 (6): 6004–6013. doi:10.1021/nn501134q

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.