Acta Biomaterialia, volume 104, pages 176-187

Neutrophil-mediated transport is crucial for delivery of short-circulating magnetic nanoparticles to tumors

Alieva Irina 2, 3
Ilyasov Artem 5
Vishnevskiy Daniil 4, 6
Chekhonin Vladimir
Majouga Alexander
Garanina Anastasiia
Melnikov Pavel A
Vodopyanov Stepan
Kapitanova Ksenia 7
Eletskaya Barbara Z
Potashnikova Daria 8
Melnikov Pavel 4, 6
Eletskaya Barbara 10
Чехонин В. П. 4, 6
Publication typeJournal Article
Publication date2020-03-01
Quartile SCImago
Q1
Quartile WOS
Q1
Impact factor9.7
ISSN17427061
Biochemistry
Molecular Biology
General Medicine
Biotechnology
Biomaterials
Biomedical Engineering
Abstract
Recently neutrophil-based nanoparticles (NPs) drug delivery systems have gained considerable attention in cancer therapy. Numerous studies have been conducted to identify optimal NPs parameters for passive tumor targeting, while there is a fundamental dearth of knowledge about the factors governing cell-mediated delivery. Here, by using intravital microscopy and magnetic resonance imaging, we describe accumulation dynamics of 140 nm magnetic cubes and clusters in murine breast cancer (4T1) and colon cancer (CT26) models. Notwithstanding rapid clearance from the blood flow, NPs readily accumulated in tumors at later time points. Both NPs types were captured mostly by intravascular neutrophils immediately after injection, and transmigration of NPs-bound neutrophils through the vessel wall was first shown in real-time. A dramatic drop in NPs accumulation upon Ly6G and Gr1 depletion further confirmed the role of neutrophils as a biocarrier for targeting tumors. Of note, for shorter circulating NPs, a cell-dependent delivery route was more impactful, while the accumulation of longer circulating counterpart was less compromised by neutrophil depletion. Neutrophil-mediated transport was also shown to depend on tumor type, with more efficiency noted in neutrophil-rich tumors. Revealing NPs characteristics and host factors influencing the neutrophil-based tumor targeting will help to rationally design drug delivery systems for improved cancer treatment. Statement of significance Utilizing host cells as trojan horses for delivery nanodrugs to tumor site is a promising approach for cancer therapy. However, it is not clear yet how nanoparticles characteristics and tumor properties affect the efficiency of cell-based nanoparticles transport. Here, we compare neutrophil-based delivery of different-shaped magnetic nanoparticles (cubes and clusters) in two tumor models. The results suggest that neutrophil-mediated route is more impactful for rapidly cleared cubes, than for longer circulating clusters. The efficiency of cell-based accumulation also correlated with the level of neutrophils recruitment to different tumor types. These finding are important for rationale design of nanocarriers and predicting the efficiency of neutrophil-mediated drug delivery between patients and tumor types.

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Naumenko V. et al. Neutrophil-mediated transport is crucial for delivery of short-circulating magnetic nanoparticles to tumors // Acta Biomaterialia. 2020. Vol. 104. pp. 176-187.
GOST all authors (up to 50) Copy
Nikitin A., Potashnikova D., Majouga A., Chekhonin V., Abakumov M. A., Eletskaya B. Z., Ilyasov A., Alieva I., Vishnevskiy D., Kapitanova K., Vodopyanov S., Melnikov P. A., Garanina A., Naumenko V., Nikitin A. A., Garanina A. S., Melnikov P., Vodopyanov S. S., Eletskaya B., Чехонин В. П., Majouga A. G. Neutrophil-mediated transport is crucial for delivery of short-circulating magnetic nanoparticles to tumors // Acta Biomaterialia. 2020. Vol. 104. pp. 176-187.
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RIS Copy
TY - JOUR
DO - 10.1016/j.actbio.2020.01.011
UR - https://doi.org/10.1016%2Fj.actbio.2020.01.011
TI - Neutrophil-mediated transport is crucial for delivery of short-circulating magnetic nanoparticles to tumors
T2 - Acta Biomaterialia
AU - Naumenko, Victor
AU - Nikitin, Aleksey
AU - Garanina, Anastasiia
AU - Melnikov, Pavel A
AU - Vodopyanov, Stepan
AU - Kapitanova, Ksenia
AU - Vishnevskiy, Daniil
AU - Alieva, Irina
AU - Ilyasov, Artem
AU - Eletskaya, Barbara Z
AU - Abakumov, Maxim A.
AU - Chekhonin, Vladimir
AU - Majouga, Alexander
AU - Potashnikova, Daria
AU - Nikitin, Aleksey A
AU - Garanina, A. S.
AU - Melnikov, Pavel
AU - Vodopyanov, Stepan S
AU - Eletskaya, Barbara
AU - Чехонин, В. П.
AU - Majouga, Alexander G.
PY - 2020
DA - 2020/03/01 00:00:00
PB - Elsevier
SP - 176-187
VL - 104
SN - 1742-7061
ER -
BibTex
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BibTex Copy
@article{2020_Naumenko
author = {Victor Naumenko and Aleksey Nikitin and Anastasiia Garanina and Pavel A Melnikov and Stepan Vodopyanov and Ksenia Kapitanova and Daniil Vishnevskiy and Irina Alieva and Artem Ilyasov and Barbara Z Eletskaya and Maxim A. Abakumov and Vladimir Chekhonin and Alexander Majouga and Daria Potashnikova and Aleksey A Nikitin and A. S. Garanina and Pavel Melnikov and Stepan S Vodopyanov and Barbara Eletskaya and В. П. Чехонин and Alexander G. Majouga},
title = {Neutrophil-mediated transport is crucial for delivery of short-circulating magnetic nanoparticles to tumors},
journal = {Acta Biomaterialia},
year = {2020},
volume = {104},
publisher = {Elsevier},
month = {mar},
url = {https://doi.org/10.1016%2Fj.actbio.2020.01.011},
pages = {176--187},
doi = {10.1016/j.actbio.2020.01.011}
}
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