journal article·2024-06Open access

Physicochemical Targeting of Lipid Nanoparticles to the Lungs Induces Clotting: Mechanisms and Solutions

Serena Omo‐Lamai, Marco E. Zamora, Manthan N. Patel, Jichuan Wu, Jia Nong, Zhicheng Wang, Alina Peshkova, Aparajeeta Majumder, Jilian R. Melamed, Liam S. Chase, Eno‐Obong Essien, Drew Weissman, Vladimir R. Muzykantov, Oscar A. Marcos‐Contreras, Jacob W. Myerson, Jacob S. Brenner

Advanced Materials· Volume 36· Issue 26

Abstract

Abstract Lipid nanoparticles (LNPs) have become the dominant drug delivery technology in industry, holding the promise to deliver RNA to up or down‐regulate any protein of interest. LNPs have mostly been targeted to specific cell types or organs by physicochemical targeting in which LNP’s lipid compositions are adjusted to find mixtures with the desired tropism. Here lung‐tropic LNPs are examined, whose organ tropism derives from containing either a cationic or ionizable lipid conferring a positive zeta potential. Surprisingly, these LNPs are found to induce massive thrombosis. Such thrombosis is shown in the lungs and other organs, and it is shown that it is greatly exacerbated by pre‐existing inflammation. This clotting is induced by a variety of formulations with cationic lipids, including LNPs and non‐LNP nanoparticles, and even by lung‐tropic ionizable lipids that do not have a permanent cationic charge. The mechanism depends on the LNPs binding to and then changing the conformation of fibrinogen, which then activates platelets and thrombin. Based on these mechanisms, multiple solutions are engineered that enable positively charged LNPs to target the lungs while ameliorating thrombosis. The findings illustrate how physicochemical targeting approaches must be investigated early for risks and re‐engineered with a careful understanding of biological mechanisms.
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Research context

OpenAlex topics: Platelet Disorders and Treatments · Inhalation and Respiratory Drug Delivery · Blood properties and coagulation

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Bioengineering University of Pennsylvania Philadelphia PA 19104 USA

School of Biomedical Engineering Drexel University Philadelphia PA 19104 USA

Department of Systems Pharmacology and Translational Therapeutics Perelman School of Medicine University of Pennsylvania Philadelphia PA 19104 USA

Division of Pulmonary Allergy, and Critical Care Department of Medicine Perelman School of Medicine University of Pennsylvania Philadelphia PA 19104 USA

Department of Medicine Perelman School of Medicine University of Pennsylvania Philadelphia PA 19104 USA

Funding

American Heart Association · Pharmaceutical Research and Manufacturers of America Foundation

References (44)

Show source-provided references
1. 10.1038/s41573-021-00283-510.1038/s41573-021-00283-5 ↗
2. 10.1016/j.jconrel.2018.10.01510.1016/j.jconrel.2018.10.015 ↗
3. 10.1126/sciadv.abf439810.1126/sciadv.abf4398 ↗
4. 10.1038/mt.2010.8510.1038/mt.2010.85 ↗
5. 10.1038/s41565-020-0669-610.1038/s41565-020-0669-6 ↗
6. 10.1038/nature1830010.1038/nature18300 ↗
7. 10.1021/jacs.1c0958510.1021/jacs.1c09585 ↗
8. 10.1073/pnas.210925611810.1073/pnas.2109256118 ↗
9. 10.1016/j.jconrel.2022.03.04610.1016/j.jconrel.2022.03.046 ↗
10. Blake T. R. · Bioconjug. Chem. · 2023 · 34 · 673
11. 10.1021/acs.nanolett.8b0291710.1021/acs.nanolett.8b02917 ↗
12. 10.1021/acs.biomac.7b0135610.1021/acs.biomac.7b01356 ↗
13. 10.1038/s41565-021-00997-y10.1038/s41565-021-00997-y ↗
14. 10.1002/adma.20210707010.1002/adma.202107070 ↗
15. 10.3390/nano1004078710.3390/nano10040787 ↗
16. 10.1016/j.biomaterials.2017.11.04010.1016/j.biomaterials.2017.11.040 ↗
17. 10.2217/nnm.13.4910.2217/nnm.13.49 ↗
18. 10.1021/mp200605410.1021/mp2006054 ↗
19. 10.1016/j.nano.2011.12.00110.1016/j.nano.2011.12.001 ↗
20. 10.3390/cells810120910.3390/cells8101209 ↗
21. 10.2174/092986732366616010615142810.2174/0929867323666160106151428 ↗
22. 10.1016/j.ijpharm.2023.12336910.1016/j.ijpharm.2023.123369 ↗
23. 10.1160/TH12-08-063410.1160/TH12-08-0634 ↗
24. 10.1073/pnas.211627111910.1073/pnas.2116271119 ↗
25. 10.1182/blood-2017-04-56911110.1182/blood-2017-04-569111 ↗
26. 10.1016/j.blre.2020.10073310.1016/j.blre.2020.100733 ↗
27. 10.1002/cpz1.17810.1002/cpz1.178 ↗
28. 10.1016/S0021-9150(96)05980-110.1016/S0021-9150(96)05980-1 ↗
29. 10.1039/D2LC00799A10.1039/D2LC00799A ↗
30. 10.1016/j.jconrel.2023.06.01410.1016/j.jconrel.2023.06.014 ↗
31. 10.1111/jth.1278510.1111/jth.12785 ↗
32. 10.1021/ja037263o10.1021/ja037263o ↗
33. 10.1038/s41598-018-37621-410.1038/s41598-018-37621-4 ↗
34. 10.1021/nn302995310.1021/nn3029953 ↗
35. 10.1038/nnano.2010.25010.1038/nnano.2010.250 ↗
36. 10.1016/S0092-8674(00)80983-610.1016/S0092-8674(00)80983-6 ↗
37. 10.1182/blood.V120.21.384.38410.1182/blood.V120.21.384.384 ↗
38. 10.1186/1477-9560-5-510.1186/1477-9560-5-5 ↗
39. 10.3324/haematol.2017.18297210.3324/haematol.2017.182972 ↗
40. 10.1039/C7OB01058C10.1039/C7OB01058C ↗
41. 10.1111/j.1538-7836.2011.04339.x10.1111/j.1538-7836.2011.04339.x ↗
42. 10.1021/la502566810.1021/la5025668 ↗
43. 10.1016/j.jconrel.2021.12.02710.1016/j.jconrel.2021.12.027 ↗
44. 10.1073/pnas.191201211710.1073/pnas.1912012117 ↗