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Amniotic fluid stabilized lipid nanoparticles for in utero intra-amniotic mRNA delivery

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Swingle, Kelsey L., Billingsley, Margaret M., Bose, Sourav K., White, Brandon, Palanki, Rohan, Dave, Apeksha, Patel, Savan K., Gong, Ningqiang +5 more·2022·Journal of Controlled Release
DOI 10.1016/j.jconrel.2021.10.031PMC PMC8776620
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Abstract

Congenital disorders resulting in pathological protein deficiencies are most often treated postnatally with protein or enzyme replacement therapies. However, treatment of these disorders in utero before irreversible disease onset could significantly minimize disease burden, morbidity, and mortality. One possible strategy for the prenatal treatment of congenital disorders is in utero delivery of messenger RNA (mRNA). mRNA is a nucleic acid therapeutic that has previously been investigated as a platform for protein replacement therapies and gene editing technologies. While viral vectors have been explored to induce intracellular expression of mRNA, they are limited in their clinical application due to risks associated with immunogenicity and genomic integration. As an alternative to viral vectors, safe and efficient in utero mRNA delivery can be achieved using ionizable lipid nanoparticles (LNPs). While LNPs have demonstrated potent in vivo mRNA delivery to the liver following intravenous administration, intra-amniotic delivery has the potential to deliver mRNA to cells and tissues beyond those in the liver, such as in the skin, lung, and digestive tract. However, LNP stability in fetal amniotic fluid and how this stability affects mRNA delivery has not been previously investigated. Here, we engineered a library of LNPs using orthogonal design of experiments (DOE) to evaluate how LNP structure affects their stability in amniotic fluid ex utero and whether a lead candidate identified from these stability measurements enables intra-amniotic mRNA delivery in utero. We used a combination of techniques including dynamic light scattering (DLS), transmission electron microscopy (TEM), and chromatography followed by protein content quantification to screen LNP stability in amniotic fluids. These results identified multiple lead LNP formulations that are highly stable in amniotic fluids ranging from small animals to humans, including mouse, sheep, pig, and human amniotic fluid samples. We then demonstrate that stable LNPs from the ex utero screen in mouse amniotic fluid enabled potent mRNA delivery in primary fetal lung fibroblasts and in utero following intra-amniotic injection in a murine model. This exploration of ex utero stability in amniotic fluids demonstrates a means by which to identify novel LNP formulations for prenatal treatment of congenital disorders via in utero mRNA delivery.

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  • The molar ratios at which LNP components are combined can be optimized for specific applications to better encapsulate nucleic acid cargo, enhance uptake by target cells, or alter biodistribution and protein corona formation.

    “The molar ratios at which the components of LNPs are combined can be optimized for specific applications to better encapsulate nucleic acid cargo, enhance uptake by target cells, or alter biodistribution and protein corona formation (28).”

    From Ionizable Lipid Nanoparticles for Therapeutic Base Editing of Congenital Brain Disease (2023) · cites this paper as [28]

    The Introduction and Discussion state that LNP component ratios can be optimized for delivery and biodistribution, and that lipid-to-cargo ratios can improve encapsulation. The Results link excipient ratios to mRNA delivery, but do not measure target-cell uptake. The Discussion treats differences in protein corona formation as a hypothesis requiring future study, not an established effect of changing molar ratios. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Modulating excipient molar ratios improves in vitro delivery to fetal lung cells and corresponds to enhanced in vivo performance following intra-amniotic LNP injection.

    “In prior work, we demonstrated that modulating excipient molar ratios improves in vitro delivery to fetal lung cells and corresponds to enhanced in vivo performance following intra-amniotic LNP injection (28).”

    From Ionizable Lipid Nanoparticles for Therapeutic Base Editing of Congenital Brain Disease (2023) · cites this paper as [28]

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Cited by

Sorted by citations

Authors
Swingle, K. L., Billingsley, M. M., Bose, S. K., White, B., Palanki, R., Dave, A., Patel, S. K., Gong, N., Hamilton, A. G., Alameh, M.-G., Weissman, D., Peranteau, W. H., & Mitchell, M. J.
Affiliations
  • University of Pennsylvania (US)
  • Children's Hospital of Philadelphia (US)
  • Abramson Cancer Center (US)
Corresponding author
  • Peranteau, William H.
  • Mitchell, Michael J.
ORCID
Venue
Journal of Controlled Release
Publisher
Elsevier BV
Published
2022-01
Volume
341
Pages
616-633
ISSN
0168-3659 (ISSN-L)
DOI
10.1016/j.jconrel.2021.10.031
PMC
PMC8776620
OpenAlex
W3210039809
Cited by
64
References
10
Citations by year
2026: 7 · 2025: 16 · 2024: 17 · 2023: 19 · 2022: 5
FWCI
3.22
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Controlled Release (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (DP2TR002776)
  • National Heart, Lung, and Blood Institute (R01HL151352, DP2HL152427)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK123049)
  • National Center for Advancing Translational Sciences
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Interference and Gene Delivery
  • Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
  • Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmaceutical Science › Advanced Drug Delivery Systems
Keywords
lipid nanoparticles, amniotic fluid, intra-amniotic injection, fetal therapy, congenital disorders, protein replacement therapy, fetal lung fibroblasts, mouse model
MeSH terms
Amniotic Fluid, Animals, Liposomes, RNA, Messenger, Sheep, Swine, Mice, Nanoparticles

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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