Geometrically constrained cytoskeletal reorganisation modulates DNA nanostructures uptake

. 2025 Feb 12 ; 13 (7) : 2335-2351. [epub] 20250212

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39835937

Grantová podpora
DP2 GM132931 NIGMS NIH HHS - United States
R01 GM145916 NIGMS NIH HHS - United States

DNA nanostructures (DNs) have gained popularity in various biomedical applications due to their unique properties, including structural programmability, ease of synthesis and functionalization, and low cytotoxicity. Effective utilization of DNs in biomedical applications requires a fundamental understanding of their interactions with living cells and the mechanics of cellular uptake. Current knowledge primarily focuses on how the physicochemical properties of DNs, such as mass, shape, size, and surface functionalization, affect uptake efficacy. However, the role of cellular mechanics and morphology in DN uptake remains largely unexplored. In this work, we show that cells subjected to geometric constraints remodel their actin cytoskeleton, resulting in differential mechanical force generation that facilitates DN uptake. The length, number, and orientation of F-actin fibers are influenced by these constraints, leading to distinct mechanophenotypes. Overall, DN uptake is governed by F-actin forces arising from filament reorganisation under geometric constraints. These results underscore the importance of actin dynamics in the cellular uptake of DNs and suggest that leveraging geometric constraints to induce specific cell morphology adaptations could enhance the uptake of therapeutically designed DNs.

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Ginzberg M. B. et al. . Science. 2015;348:1245075. doi: 10.1126/science.1245075. PubMed DOI PMC

Lloyd A. C. Cell. 2013;154:1194–1205. doi: 10.1016/j.cell.2013.08.053. PubMed DOI

Bao M. et al. . Nat. Commun. 2017;8:1962. doi: 10.1038/s41467-017-02163-2. PubMed DOI PMC

Wang X. L. et al. . Biomater. Sci. 2016;4:970–978. doi: 10.1039/C6BM00171H. PubMed DOI

Khetan J. et al. . Biophys. J. 2019;116:347–359. doi: 10.1016/j.bpj.2018.11.3134. PubMed DOI PMC

Elblová P. et al. . Discover Nano. 2024;19:106. doi: 10.1186/s11671-024-04052-2. PubMed DOI PMC

Shin H. et al. . Nanoscale. 2020;12:15743–15751. doi: 10.1039/D0NR01627F. PubMed DOI

Amodeo A. A. et al. . Cold Spring Harbor Perspect. Biol. 2016;8:a019083. doi: 10.1101/cshperspect.a019083. PubMed DOI PMC

Lindemann C. et al. . Front. Mar. Sci. 2016;3:26.

Rupprecht J. F. et al. . Mol. Biol. Cell. 2017;28:3582–3594. doi: 10.1091/mbc.e17-01-0060. PubMed DOI PMC

Lunova M. et al. . Integr. Biol. 2016;8:1099–1110. doi: 10.1039/C6IB00125D. PubMed DOI

Vogel V. et al. . Nat. Rev. Mol. Cell Biol. 2006;7:265–275. doi: 10.1038/nrm1890. PubMed DOI

Bidhendi A. J. et al. . Nat. Commun. 2023;14:8275. doi: 10.1038/s41467-023-44075-4. PubMed DOI PMC

Versaevel M. et al. . Nat. Commun. 2012;3:671. doi: 10.1038/ncomms1668. PubMed DOI

Jain N. et al. . Proc. Natl. Acad. Sci. U. S. A. 2013;110:11349–11354. doi: 10.1073/pnas.1300801110. PubMed DOI PMC

Li Y. W. et al. . Matter. 2021;4:1863–1891. doi: 10.1016/j.matt.2021.03.013. PubMed DOI PMC

Chen C. S. et al. . Science. 1997;276:1425–1428. doi: 10.1126/science.276.5317.1425. PubMed DOI

Fattahi P. et al. . Adv. Mater. Interfaces. 2023;10:2300137. doi: 10.1002/admi.202300137. DOI

Rennick J. J. et al. . Nat. Nanotechnol. 2021;16:266–276. doi: 10.1038/s41565-021-00858-8. PubMed DOI

Zhang S. L. et al. . ACS Nano. 2015;9:8655–8671. doi: 10.1021/acsnano.5b03184. PubMed DOI PMC

Muoth C. et al. . RSC Adv. 2016;6:72827–72835. doi: 10.1039/C6RA13782B. DOI

Ladoux B. et al. . Nat. Rev. Mol. Cell Biol. 2017;18:743–757. doi: 10.1038/nrm.2017.98. PubMed DOI

Atia L. et al. . Nat. Phys. 2018;14:613–620. PubMed PMC

Dupont S. et al. . Nat. Rev. Genet. 2022;23:624–643. doi: 10.1038/s41576-022-00493-6. PubMed DOI

Massey A. et al. . Nat. Rev. Phys. 2024;6:269–282. doi: 10.1038/s42254-024-00707-2. PubMed DOI PMC

Romani P. et al. . Nat. Cell Biol. 2024;26:2046–2060. doi: 10.1038/s41556-024-01527-3. PubMed DOI PMC

Keller A. et al. . Angew. Chem., Int. Ed. 2020;59:15818–15833. doi: 10.1002/anie.201916390. PubMed DOI PMC

Jahanban-Esfahlan A. et al. . J. Controlled Release. 2019;315:166–185. doi: 10.1016/j.jconrel.2019.10.003. PubMed DOI

Henry S. J. W. et al. . Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2021;13:e1729. PubMed PMC

Dey S. et al. . Nat. Rev. Methods Primers. 2021;1:13. doi: 10.1038/s43586-020-00009-8. DOI

Wang J. et al. . Nat. Rev. Mater. 2021;6:766–783. doi: 10.1038/s41578-021-00315-x. PubMed DOI PMC

Simmons C. R. et al. . Angew. Chem., Int. Ed. 2020;59:18619–18626. doi: 10.1002/anie.202005505. PubMed DOI

Frtus A. et al. . Acta Biomater. 2022;146:10–22. doi: 10.1016/j.actbio.2022.04.046. PubMed DOI PMC

Tian T. R. et al. . Bone Res. 2022;10:40. doi: 10.1038/s41413-022-00212-1. PubMed DOI PMC

Xu R. et al. . Adv. NanoBiomed Res. 2023;3:2200119. doi: 10.1002/anbr.202200119. DOI

Wang W. T. et al. . Nano Lett. 2023;23:7076–7085. doi: 10.1021/acs.nanolett.3c01878. PubMed DOI PMC

Wang W. T. et al. . ACS Appl. Mater. Interfaces. 2024;16:15783–15797. doi: 10.1021/acsami.3c18068. PubMed DOI PMC

Wang P. et al. . J. Am. Chem. Soc. 2018;140:2478–2484. doi: 10.1021/jacs.7b09024. PubMed DOI PMC

Bastings M. M. C. et al. . Nano Lett. 2018;18:3557–3564. doi: 10.1021/acs.nanolett.8b00660. PubMed DOI

Whitehouse W. L. et al. . Bioconjugate Chem. 2019;30:1836–1844. doi: 10.1021/acs.bioconjchem.9b00036. PubMed DOI

Balakrishnan D. et al. . Nanomedicine. 2019;14:911–925. doi: 10.2217/nnm-2018-0440. PubMed DOI

Wang P. F. et al. . Chem. 2017;2:359–382.

Mikkila J. et al. . Nano Lett. 2014;14:2196–2200. doi: 10.1021/nl500677j. PubMed DOI

Liu K. et al. . J. Mater. Chem. B. 2020;8:6802–6809. doi: 10.1039/D0TB00663G. PubMed DOI

Arulkumaran N. et al. . ACS Nano. 2021;15:4394–4404. doi: 10.1021/acsnano.0c07915. PubMed DOI

Maezawa T. et al. . Nanoscale. 2020;12:14818–14824. doi: 10.1039/D0NR02361B. PubMed DOI

Lee D. S. et al. . Chem. Soc. Rev. 2016;45:4199–4225. doi: 10.1039/C5CS00700C. PubMed DOI

Mosquera J. et al. . Acc. Chem. Res. 2018;51:2305–2313. doi: 10.1021/acs.accounts.8b00292. PubMed DOI

Behzadi S. et al. . Chem. Soc. Rev. 2017;46:4218–4244. doi: 10.1039/C6CS00636A. PubMed DOI PMC

Lunov O. et al. . ACS Nano. 2011;5:1657–1669. doi: 10.1021/nn2000756. PubMed DOI

Donahue N. D. et al. . Adv. Drug Delivery Rev. 2019;143:68–96. doi: 10.1016/j.addr.2019.04.008. PubMed DOI

Smolková B. et al. . ACS Appl. Mater. Interfaces. 2021;13:46375–46390. doi: 10.1021/acsami.1c14401. PubMed DOI PMC

Rajwar A. et al. . ACS Nano. 2022;16:10496–10508. doi: 10.1021/acsnano.2c01382. PubMed DOI

Mathur D. et al. . Nano Lett. 2022;22:5037–5045. doi: 10.1021/acs.nanolett.2c00917. PubMed DOI PMC

Peng Y. A. et al. . Adv. Sci. 2023;10:2300614. doi: 10.1002/advs.202300614. PubMed DOI PMC

Elblová P. et al. . Chem. Eng. J. 2024;498:155633. doi: 10.1016/j.cej.2024.155633. PubMed DOI PMC

Ngo W. et al. . Adv. Drug Delivery Rev. 2022;185:114238. doi: 10.1016/j.addr.2022.114238. PubMed DOI

Frtús A. et al. . J. Controlled Release. 2020;328:59–77. doi: 10.1016/j.jconrel.2020.08.036. PubMed DOI

Tsoi K. M. et al. . Nat. Mater. 2016;15:1212–1221. doi: 10.1038/nmat4718. PubMed DOI PMC

Uzhytchak M. et al. . Adv. Drug Delivery Rev. 2023;197:114828. doi: 10.1016/j.addr.2023.114828. PubMed DOI

Schulze R. J. et al. . J. Cell Biol. 2019;218:2096–2112. doi: 10.1083/jcb.201903090. PubMed DOI PMC

Fernandez-Checa J. C. et al. . J. Hepatol. 2021;75:935–959. doi: 10.1016/j.jhep.2021.06.021. PubMed DOI

Andrade R. J. et al. . Nat. Rev. Dis. Primers. 2019;5:58. doi: 10.1038/s41572-019-0105-0. PubMed DOI

Guo L. et al. . Drug Metab. Dispos. 2011;39:528–538. doi: 10.1124/dmd.110.035873. PubMed DOI PMC

Arzumanian V. A. et al. . Int. J. Mol. Sci. 2021;22:13135. doi: 10.3390/ijms222313135. PubMed DOI PMC

Fukuyama K. et al. . PLoS One. 2021;16:e0245939. doi: 10.1371/journal.pone.0245939. PubMed DOI PMC

Lunova M. et al. . Cell. Mol. Life Sci. 2020;77:2815–2838. doi: 10.1007/s00018-019-03321-z. PubMed DOI PMC

Kroemer G. et al. . Cell Death Differ. 2009;16:3–11. doi: 10.1038/cdd.2008.150. PubMed DOI PMC

Crowley L. C. et al. . Cold Spring Harb. Protoc. 2016;2016:647–651. PubMed

Frtus A. et al. . ACS Biomater. Sci. Eng. 2023;9:2408–2425. doi: 10.1021/acsbiomaterials.2c01518. PubMed DOI PMC

de Chaumont F. et al. . Nat. Methods. 2012;9:690–696. doi: 10.1038/nmeth.2075. PubMed DOI

Suzuki H. et al. . Environ. Sci. Technol. 2007;41:3018–3024. doi: 10.1021/es0625632. PubMed DOI

Uzhytchak M. et al. . Cells. 2020;9:1015. doi: 10.3390/cells9041015. PubMed DOI PMC

Torrano A. A. et al. . Nanomedicine. 2013;8:1815–1828. doi: 10.2217/nnm.12.178. PubMed DOI

Blechinger J. et al. . Small. 2013;9:3970–3980. doi: 10.1002/smll.201301004. PubMed DOI

Arganda-Carreras I. et al. . Microsc. Res. Tech. 2010;73:1019–1029. doi: 10.1002/jemt.20829. PubMed DOI

Rezakhaniha R. et al. . Biomech. Model. Mechanobiol. 2012;11:461–473. doi: 10.1007/s10237-011-0325-z. PubMed DOI

Mogilner A. et al. . Biophys. J. 2003;84:1591–1605. doi: 10.1016/S0006-3495(03)74969-8. PubMed DOI PMC

Martiel J. L. et al. . Biophys. J. 2020;118:182–192. doi: 10.1016/j.bpj.2019.10.039. PubMed DOI PMC

Dolati S. et al. . Mol. Biol. Cell. 2018;29:2674–2686. doi: 10.1091/mbc.E18-02-0082. PubMed DOI PMC

Koudehi M. A. et al. . Cytoskeleton. 2019;76:532–548. doi: 10.1002/cm.21565. PubMed DOI PMC

Falcke M. Phys. D. 2016;318:50–57. doi: 10.1016/j.physd.2015.10.019. DOI

Gupta M. et al. . Nat. Commun. 2015;6:7525. doi: 10.1038/ncomms8525. PubMed DOI PMC

Sakamoto R. et al. . Nat. Commun. 2024;15:3444. doi: 10.1038/s41467-024-47593-x. PubMed DOI PMC

Chen X. D. et al. . Commun. Biol. 2020;3:616. doi: 10.1038/s42003-020-01335-z. PubMed DOI PMC

Shi C. et al. . EURASIP J. Wirel. Commun. Netw. 2021;2021:31. doi: 10.1186/s13638-021-01910-w. PubMed DOI PMC

Hamilton N. Traffic. 2009;10:951–961. doi: 10.1111/j.1600-0854.2009.00938.x. PubMed DOI

Jonkman J. et al. . Nat. Protoc. 2020;15:1585–1611. doi: 10.1038/s41596-020-0313-9. PubMed DOI

Lee J. Y. et al. . Mol. Biol. Cell. 2018;29:1519–1525. doi: 10.1091/mbc.E17-05-0276. PubMed DOI PMC

Uzhytchak M. et al. . Sci. Rep. 2023;13:10818. doi: 10.1038/s41598-023-38015-x. PubMed DOI PMC

Dell R. B. et al. . ILAR J. 2002;43:207–213. doi: 10.1093/ilar.43.4.207. PubMed DOI PMC

Birkholz O. et al. . Nat. Commun. 2018;9:1521. doi: 10.1038/s41467-018-02905-w. PubMed DOI PMC

Burns J. R. et al. . ACS Nano. 2018;12:3263–3271. doi: 10.1021/acsnano.7b07835. PubMed DOI

Burns J. R. et al. . Nat. Nanotechnol. 2016;11:152–156. doi: 10.1038/nnano.2015.279. PubMed DOI

Zhang Y. L. et al. . ACS Nano. 2023;17:10486–10495. doi: 10.1021/acsnano.3c01342. PubMed DOI PMC

Long Q. P. et al. . ACS Appl. Mater. Interfaces. 2021;13:47987–47995. doi: 10.1021/acsami.1c15585. PubMed DOI

Mei Q. A. et al. . Nano Lett. 2011;11:1477–1482. doi: 10.1021/nl1040836. PubMed DOI PMC

Keum J. W. et al. . Chem. Commun. 2009:7036–7038. doi: 10.1039/B917661F. PubMed DOI

Massich M. D. et al. . ACS Nano. 2010;4:5641–5646. doi: 10.1021/nn102228s. PubMed DOI PMC

Shen X. B. et al. . Chem. Commun. 2012;48:11301–11303. doi: 10.1039/C2CC36185J. PubMed DOI

Walsh A. S. et al. . ACS Nano. 2011;5:5427–5432. doi: 10.1021/nn2005574. PubMed DOI

Li P. et al. . Int. J. Nanomed. 2012;7:925–939. PubMed PMC

Mendes B. B. et al. . Nat. Rev. Methods Primers. 2022;2:24. doi: 10.1038/s43586-022-00104-y. PubMed DOI PMC

Dilliard S. A. et al. . Nat. Rev. Mater. 2023;8:282–300. doi: 10.1038/s41578-022-00529-7. PubMed DOI PMC

Prasad R. Y. et al. . ACS Nano. 2013;7:1929–1942. doi: 10.1021/nn302280n. PubMed DOI

Salvati A. et al. . Nanoimpact. 2018;9:42–50. doi: 10.1016/j.impact.2017.10.004. DOI

Bolte S. et al. . J. Microsc. 2006;224:213–232. doi: 10.1111/j.1365-2818.2006.01706.x. PubMed DOI

Chen H. H. et al. . J. Nanobiotechnol. 2011;9:14. doi: 10.1186/1477-3155-9-14. PubMed DOI PMC

Elsaesser A. et al. . Nanomedicine. 2010;5:1447–1457. doi: 10.2217/nnm.10.118. PubMed DOI

Qiu Z. X. et al. . Sci. Rep. 2016;6:27411. doi: 10.1038/srep27411. PubMed DOI PMC

Septiadi D. et al. . Adv. Mater. 2018;30:1704463. doi: 10.1002/adma.201704463. PubMed DOI

Rees P. et al. . Nat. Commun. 2019;10:2341. doi: 10.1038/s41467-019-10112-4. PubMed DOI PMC

Ishikawa J. et al. . Commun. Biol. 2021;4:409. doi: 10.1038/s42003-021-01936-2. PubMed DOI PMC

Baiocchini A. et al. , in Hepatocellular Carcinoma, ed. G. M. Ettorre, Springer International Publishing, Cham, 2023, pp. 45–5210.1007/978-3-031-09371-5_6 DOI

Lacroix A. et al. . ACS Cent. Sci. 2019;5:882–891. doi: 10.1021/acscentsci.9b00174. PubMed DOI PMC

Chandrasekaran A. R. Nat. Rev. Chem. 2021;5:225–239. doi: 10.1038/s41570-021-00251-y. PubMed DOI PMC

Letort G. et al. . F1000Res. 2015;4:940. PubMed PMC

Papakonstanti E. A. et al. . FEBS Lett. 2008;582:2120–2127. doi: 10.1016/j.febslet.2008.02.064. PubMed DOI

Fletcher D. A. et al. . Nature. 2010;463:485–492. doi: 10.1038/nature08908. PubMed DOI PMC

Nel A. E. et al. . Nat. Mater. 2009;8:543–557. doi: 10.1038/nmat2442. PubMed DOI

Svitkina T. Cold Spring Harbor Perspect. Biol. 2018;10:a018267. doi: 10.1101/cshperspect.a018267. PubMed DOI PMC

Clarke D. N. et al. . Curr. Biol. 2021;31:R667–R680. doi: 10.1016/j.cub.2021.03.031. PubMed DOI PMC

Wu L. G. et al. . Front. Synaptic Neurosci. 2022;14:841704. doi: 10.3389/fnsyn.2022.841704. PubMed DOI PMC

van der Meel R. et al. . Expert Opin. Drug Delivery. 2017;14:1–5. doi: 10.1080/17425247.2017.1262346. PubMed DOI PMC

Dawson K. A. et al. . Nat. Nanotechnol. 2021;16:229–242. doi: 10.1038/s41565-021-00860-0. PubMed DOI

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