Genetically Controlled Iron Oxide Biomineralization in Encapsulin Nanocompartments for Magnetic Manipulation of a Mammalian Cell Line
Abstract Magnetic nanoparticles have proven invaluable for biomechanical investigations due to their ability to exert localized forces. However, cellular delivery of exogenous magnetic agents often results in endosomal entrapment, thereby limiting their utility for manipulating subcellular structures. This study characterizes and exploits fully genetically controlled biomineralization of iron‐oxide cores inside encapsulin nanocompartments to enable magnetic‐activated cell sorting (MACS) and magnetic cell manipulation. The fraction of MACS‐retained cells showed substantial overexpression of encapsulins and exhibited both para‐ and ferrimagnetic responses with magnetic moments of 10 −15 A m 2 per cell, comparable to standard exogenous labels for MACS. Electron microscopy revealed that MACS‐retained cells contained densely packed agglomerates of ≈30 nm iron oxide cores consisting of ultrafine quasicrystalline ordered nuclei within an amorphous matrix of iron, oxygen, and phosphorus. Scanning transmission X‐ray microscopy, X‐ray absorption spectroscopy, and Raman microspectroscopy confirmed that the iron‐oxide species are consistent with ferric oxide (Fe 2 O 3 ). In addition, the encapsulin‐overexpressing MACS‐retained cells can be manipulated by a magnetic needle and regrown in patterns determined by magnetic gradients. This study demonstrates that the formation of quasicrystalline iron oxide with mixed para/ferrimagnetic behavior in the cytosol of mammalian cells enables magnetic manipulation without the delivery of exogenous agents.
Authors
- R. Meckenstock (ORCID: https://orcid.org/0009-0002-6537-0646)
- Michael Winklhofer (ORCID: https://orcid.org/0000-0003-1352-9723)
- Maxim A. Abakumov (ORCID: https://orcid.org/0000-0003-2622-9201)
- Anastasiia S. Garanina (ORCID: https://orcid.org/0000-0003-3442-9553)
- Franziska Curdt
- Ulf Wiedwald (ORCID: https://orcid.org/0000-0002-3209-4078)
- Michael Farle (ORCID: https://orcid.org/0000-0002-1864-3261)
- Natalia P. Ivleva (ORCID: https://orcid.org/0000-0002-7685-5166)
- Maria V. Efremova (ORCID: https://orcid.org/0000-0002-5196-5596)
- Nicolas Josten (ORCID: https://orcid.org/0009-0005-8543-8603)
- Gil G. Westmeyer (ORCID: https://orcid.org/0000-0001-7224-8919)
- Alevtina S. Semkina
- Jeroen Francke
- Irina B. Alieva (ORCID: https://orcid.org/0000-0002-5726-4889)
- Felix Sigmund
- Hendrik Ohldag (ORCID: https://orcid.org/0000-0002-2034-878X)
- Thomas Feggeler (ORCID: https://orcid.org/0000-0003-1817-2276)
- Irina Beer
- Sebastian Wintz (ORCID: https://orcid.org/0000-0001-6138-8078)
- Reinoud Lavrijsen (ORCID: https://orcid.org/0000-0002-1209-5858)
- Silviu‐Vasile Bodea
- Lorenz N. Panzl
Institutions
- National University of Science and Technology (RU)
- Carl von Ossietzky Universität Oldenburg (DE)
- Lawrence Berkeley National Laboratory (US)
- University of California, Santa Cruz (US)
- Lomonosov Moscow State University (RU)
- Helmholtz Zentrum München (DE)
- Pirogov Russian National Research Medical University (RU)
- Max Planck Institute for Intelligent Systems (DE)
- Material Sciences (United States) (US)
- University of Duisburg-Essen (DE)
- Technical University of Munich (DE)
- Eindhoven University of Technology (NL)
- University of California, Berkeley (US)
- Stanford University (US)
Publication Details
- Journal
- Advanced Functional Materials
- Published
- 2025-01-16
- DOI
- https://doi.org/10.1002/adfm.202418013
- Citations
- 5
- Primary Topic
- Geomagnetism and Paleomagnetism Studies
- Type
- article
- Field-Weighted Citation Impact
- 4.03
Funders
- U.S. Department of Energy
- Alexander von Humboldt-Stiftung
- Joachim Herz Stiftung
- European Commission
- Deutsche Forschungsgemeinschaft
- Russian Science Foundation
- Office of Science