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Red blood cell-hitchhiking boosts delivery of nanocarriers to chosen organs by orders of magnitude

Brenner, Jacob S., Pan, Daniel C., Myerson, Jacob W., Marcos-Contreras, Oscar A., Villa, Carlos H., Patel, Priyal, Hekierski, Hugh, Chatterjee, Shampa, Tao, Jian-Qin, Parhiz, Hamideh, Bhamidipati, Kartik, Uhler, Thomas G., Hood, Elizabeth D., Kiseleva, Raisa Yu., Shuvaev, Vladimir S., Shuvaeva, Tea, Khoshnejad, Makan, Johnston, Ian, Gregory, Jason V., Lahann, Joerg, Wang, Tao, Cantu, Edward, Armstead, William M., Mitragotri, Samir, Muzykantov, Vladimir·2018·Nature Communications
DOI 10.1038/s41467-018-05079-7PMC PMC6041332
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Abstract

Drug delivery by nanocarriers (NCs) has long been stymied by dominant liver uptake and limited target organ deposition, even when NCs are targeted using affinity moieties. Here we report a universal solution: red blood cell (RBC)-hitchhiking (RH), in which NCs adsorbed onto the RBCs transfer from RBCs to the first organ downstream of the intravascular injection. RH improves delivery for a wide range of NCs and even viral vectors. For example, RH injected intravenously increases liposome uptake in the first downstream organ, lungs, by ~40-fold compared with free NCs. Intra-carotid artery injection of RH NCs delivers >10% of the injected NC dose to the brain, ~10× higher than that achieved with affinity moieties. Further, RH works in mice, pigs, and ex vivo human lungs without causing RBC or end-organ toxicities. Thus, RH is a clinically translatable platform technology poised to augment drug delivery in acute lung disease, stroke, and several other diseases.

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  1. Gelpi, A., Gilbertson, A. & Tucker, J. D. Magic bullet: Paul Ehrlich, Salvarsan and the birth of venereology. Sex. Transm. Infect. 91, 68–69 (2015).
  2. Gustafson, H. H., Holt-Casper, D., Grainger, D. W. & Ghandehari, H. Nanoparticle uptake: the phagocyte problem. Nano Today 10, 487–510 (2015). · DOI
  3. Wiley, D. T., Webster, P., Gale, A. & Davis, M. E. Transcytosis and brain uptake of transferrin-containing nanoparticles by tuning avidity to transferrin receptor. Proc. Natl Acad. Sci. USA 110, 8662–8667 (2013). · DOI
  4. Villa, C. H. et al. Delivery of drugs bound to erythrocytes: new avenues for an old intravascular carrier. Ther. Deliv. 6, 795–826 (2015). · DOI
  5. Magnani, M. & Rossi, L. Approaches to erythrocyte-mediated drug delivery. Expert Opin. Drug. Deliv. 11, 677–687 (2014). · DOI
  6. Chessa, L. et al. Intra-erythrocyte infusion of dexamethasone reduces neurological symptoms in ataxia teleangiectasia patients: results of a phase 2 trial. Orphanet. J. Rare. Dis. 9, 5 (2014). · DOI
  7. Nardin, A., Lindorfer, M. A. & Taylor, R. P. How are immune complexes bound to the primate erythrocyte complement receptor transferred to acceptor phagocytic cells? Mol. Immunol. 36, 827–835 (1999). · DOI
  8. Gyimesi, E. et al. Staphylococcus aureus bound to complement receptor 1 on human erythrocytes by bispecific monoclonal antibodies is phagocytosed by acceptor macrophages. Immunol. Lett. 95, 185–192 (2004). · DOI
  9. Chu, D. et al. Nanoparticle targeting of neutrophils for improved cancer immunotherapy. Adv. Healthc. Mater. 5, 1088–1093 (2016). · DOI
  10. Anselmo, A. C. et al. Exploiting shape, cellular-hitchhiking and antibodies to target nanoparticles to lung endothelium: Synergy between physical, chemical and biological approaches. Biomaterials 68, 1–8 (2015). · DOI
  11. Anselmo, A. C. et al. Delivering nanoparticles to lungs while avoiding liver and spleen through adsorption on red blood cells. ACS Nano 7, 11129–11137 (2013). · DOI · Paper page
  12. Pan, D. et al. The effect of polymeric nanoparticles on biocompatibility of carrier red blood cells. PLoS ONE 11, e0152074 (2016). · DOI
  13. Muzykantov, V. R. et al. Streptavidin facilitates internalization and pulmonary targeting of an anti-endothelial cell antibody (platelet-endothelial cell adhesion molecule 1): a strategy for vascular immunotargeting of drugs. Proc. Natl Acad. Sci. USA 96, 2379–2384 (1999). · DOI
  14. Brenner, J. S., Greineder, C., Shuvaev, V. & Muzykantov, V. Endothelial nanomedicine for the treatment of pulmonary disease. Expert Opin. Drug. Deliv. 12, 239–261 (2015). · DOI
  15. Deng, Y. et al. Improved i.p. drug delivery with bioadhesive nanoparticles. Proc. Natl Acad. Sci. USA 113, 11453–11458 (2016). · DOI
  16. Rwei, A. Y. et al. Repeatable and adjustable on-demand sciatic nerve block with phototriggerable liposomes. Proc. Natl Acad. Sci. USA 112, 15719–15724 (2015). · DOI
  17. Huang, X. et al. Protein nanocages that penetrate airway mucus and tumor tissue. Proc. Natl Acad. Sci. USA 114, E6595–E6602 (2017). · DOI · Paper page
  18. Zhang, C. et al. Strategies to enhance the distribution of nanotherapeutics in the brain. J. Control. Release 267, 232–239 (2017). · DOI
  19. Suk, J. S., Xu, Q., Kim, N., Hanes, J. & Ensign, L. M. PEGylation as a strategy for improving nanoparticle-based drug and gene delivery. Adv. Drug Deliv. Rev. 99, 28–51 (2016). · DOI · Paper page
  20. Song, E. et al. Surface chemistry governs cellular tropism of nanoparticles in the brain. Nat. Commun. 8, 15322 (2017). · DOI
  21. Vernon, M. M., Dean, D. A. & Dobson, J. DNA targeting sequence improves magnetic nanoparticle-based plasmid DNA transfection efficiency in model neurons. Int. J. Mol. Sci. 16, 19369–19386 (2015). · DOI
  22. Lin, X., Barravecchia, M., Kothari, P., Young, J. L. & Dean, D. A. β1-Na(+),K(+)-ATPase gene therapy upregulates tight junctions to rescue lipopolysaccharide-induced acute lung injury. Gene Ther. 23, 489–499 (2016). · DOI
  23. Hood, E. D. et al. Antioxidant protection by PECAM-targeted delivery of a novel NADPH-oxidase inhibitor to the endothelium in vitro and in vivo. J. Control. Release 163, 161–169 (2012). · DOI
  24. Kuebler, W. M. & Goetz, A. E. The marginated pool. Eur. Surg. Res. 34, 92–100 (2002). · DOI
  25. Schneberger, D., Aharonson-Raz, K. & Singh, B. Pulmonary intravascular macrophages and lung health: what are we missing? Am. J. Physiol. Lung Cell. Mol. Physiol. 302, L498–L503 (2012). · DOI
  26. Downey, G. P. et al. Retention of leukocytes in capillaries: role of cell size and deformability. J. Appl. Physiol. 69, 1767–1778 (1990). · DOI
  27. Doerschuk, C. M. et al. Leukocyte and platelet margination within microvasculature of rabbit lungs. J. Appl. Physiol. 68, 1956–1961 (1990). · DOI
  28. Ryan, J., Bloch, K. & Archer, S. L. Rodent models of pulmonary hypertension: harmonisation with the world health organisation’s categorisation of human PH. Int. J. Clin. Pract. Suppl. 65, 15–34 (2011). Issue 172 · DOI
  29. Brenner, J. S. et al. Mechanisms that determine nanocarrier targeting to healthy versus inflamed lung regions. Nanomedicine 13, 1495–1506 (2017). · DOI
  30. Bdeir, K. et al. Urokinase mediates fibrinolysis in the pulmonary microvasculature. Blood 96, 1820–1826 (2000). · DOI
  31. Murciano, J.-C. et al. Platelets inhibit the lysis of pulmonary microemboli. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L529–L539 (2002). · DOI
  32. Jinatongthai, P. et al. Comparative efficacy and safety of reperfusion therapy with fibrinolytic agents in patients with ST-segment elevation myocardial infarction: a systematic review and network meta-analysis. Lancet 390, 747–759 (2017). · DOI
  33. Hu, L. et al. Assessing intrarenal nonperfusion and vascular leakage in acute kidney injury with multinuclear (1) H/(19) F MRI and perfluorocarbon nanoparticles. Magn. Reson. Med. 71, 2186–2196 (2014). · DOI
  34. Sieve, I., Münster-Kühnel, A. K. & Hilfiker-Kleiner, D. Regulation and function of endothelial glycocalyx layer in vascular diseases. Vasc. Pharmacol. 100, 26–33 (2018). · DOI
  35. Xia, Z., Li, H. & Irwin, M. G. Myocardial ischaemia reperfusion injury: the challenge of translating ischaemic and anaesthetic protection from animal models to humans. Br. J. Anaesth. 117(Suppl. 2), ii44–ii62 (2016). · DOI
  36. Chamorro, Á., Dirnagl, U., Urra, X. & Planas, A. M. Neuroprotection in acute stroke: targeting excitotoxicity, oxidative and nitrosative stress, and inflammation. Lancet Neurol. 15, 869–881 (2016). · DOI · Paper page
  37. Ferrer, M. C. C. et al. Icam-1 targeted nanogels loaded with dexamethasone alleviate pulmonary inflammation. PLoS ONE 9, e102329 (2014). · DOI
  38. Reddy, M. K., Wu, L., Kou, W., Ghorpade, A. & Labhasetwar, V. Superoxide dismutase-loaded PLGA nanoparticles protect cultured human neurons under oxidative stress. Appl. Biochem. Biotechnol. 151, 565–577 (2008). · DOI
  39. Rahmani, S. & Lahann, J. Recent progress with multicompartmental nanoparticles. MRS Bull. 39, 251–257 (2014). · DOI
  40. Pan, D. C. et al. Nanoparticle properties modulate their attachment and effect on carrier red blood cells. Sci. Rep. 8, 1615 (2018). · DOI
  41. Zhang, X., Goncalves, R. & Mosser, D. M. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. 83, 14.1.1–14.1.14 (2008). · DOI
  42. Armstead, W. M. et al. RBC-coupled tPA prevents whereas tPA aggravates JNK MAPK-mediated impairment of ATP- and Ca-sensitive K channel-mediated cerebrovasodilation after cerebral photothrombosis. Transl. Stroke Res. 3, 114–121 (2012). · DOI

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Metadata

Authors
Brenner, J. S., Pan, D. C., Myerson, J. W., Marcos-Contreras, O. A., Villa, C. H., Patel, P., Hekierski, H., Chatterjee, S., Tao, J.-Q., Parhiz, H., Bhamidipati, K., Uhler, T. G., Hood, E. D., Kiseleva, R. Y., Shuvaev, V. S., Shuvaeva, T., Khoshnejad, M., Johnston, I., Gregory, J. V., Lahann, J., Wang, T., Cantu, E., Armstead, W. M., Mitragotri, S., & Muzykantov, V.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2018-07-11
Volume
9
Issue
1
ISSN
2041-1723
DOI
10.1038/s41467-018-05079-7
PMC
PMC6041332
Cited by
363
References
1
Language
en
Licence
Funders
U.S. Department of Health & Human Services | National Institutes of Health (1RO1 HL125462-02)

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