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Scaffold-Free and Label-Free Biofabrication Technology Using Levitational Assembly in a High Magnetic Field

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Scaffold-Free and Label-Free Biofabrication Technology Using Levitational Assembly in a High Magnetic Field Scaffold-free and label-free biofabrication technology using levitational assembly in a high magnetic field Citation for published version (APA): Parfenov, V. A., Mironov, V. A., van Kampen, K. A., Karalkin, P. A., Koudan, E. V., Pereira, F. DAS., Petrov, S. V., Nezhurina, E. K., Petrov, O. F., Myasnikov, M., Walboomers, F. X., Engelkamp, H., Christianen, P., Khesuani, Y. D., Moroni, L., & Mota, C. (2020). Scaffold-free and label-free biofabrication technology using levitational assembly in a high magnetic field. Biofabrication, 12(4), [045022]. https://doi.org/10.1088/1758-5090/ab7554 Document status and date: Published: 01/10/2020 DOI: 10.1088/1758-5090/ab7554 Document Version: Publisher's PDF, also known as Version of record Document license: Taverne Please check the document version of this publication: • A submitted manuscript is the version of the article upon submission and before peer-review. There can be important differences between the submitted version and the official published version of record. People interested in the research are advised to contact the author for the final version of the publication, or visit the DOI to the publisher's website. • The final author version and the galley proof are versions of the publication after peer review. • The final published version features the final layout of the paper including the volume, issue and page numbers. 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If the publication is distributed under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license above, please follow below link for the End User Agreement: www.umlib.nl/taverne-license Take down policy If you believe that this document breaches copyright please contact us at: [email protected] providing details and we will investigate your claim. Download date: 02 Oct. 2021 Biofabrication PAPER Scaffold-free and label-free biofabrication technology using levitational assembly in a high magnetic field To cite this article: Vladislav A Parfenov et al 2020 Biofabrication 12 045022 View the article online for updates and enhancements. This content was downloaded from IP address 137.120.160.121 on 22/09/2020 at 19:10 Biofabrication 12 (2020) 045022 https://doi.org/10.1088/1758-5090/ab7554 PAPER Scaffold-free and label-free biofabrication technology using RECEIVED 17 September 2019 levitational assembly in a high magnetic field REVISED 24 January 2020 1,7,8 1,7,8 2 1,3 ACCEPTED FOR PUBLICATION Vladislav A Parfenov , Vladimir A Mironov , Kenny A van Kampen , Pavel A Karalkin , 12 February 2020 Elizaveta V Koudan1, Frederico DAS Pereira1, Stanislav V Petrov1, Elizaveta K Nezhurina3, Oleg F Petrov4, 4 5 6 6 1 PUBLISHED Maxim I Myasnikov , Frank X Walboomers , Hans Engelkamp , Peter Christianen , Yusef D Khesuani , 4 August 2020 Lorenzo Moroni2 and Carlos Mota2,8 1 Laboratory for Biotechnological Research ‘3D Bioprinting Solutions’, Moscow, Russia 2 Department of Complex Tissue Regeneration, MERLN Institute for Technology-Inspired Regenerative Medicine, Maastricht University, The Netherlands 3 National Medical Research Radiological Center, Moscow, Russia 4 Joint Institute for High Temperatures, Russian Academy of Sciences, Moscow, Russia 5 Department of Biomaterials, Radboud University Medical Center, PO Box 9101, 6500 HB, Nijmegen (309), The Netherlands 6 High Field Magnet Laboratory (HFML—EMFL), Radboud University, Toernooiveld 7, 6525 ED Nijmegen, The Netherlands 7 Both authors contributed equally to this paper. 8 Authors to whom any correspondence should be addressed. E-mail: [email protected], [email protected] and [email protected] Keywords: tissue spheroids, magnetic levitation, biofabrication, high magnetic field, gadolinium salt Supplementary material for this article is available online Abstract The feasibility of magnetic levitational bioassembly of tissue-engineered constructs from living tissue + + spheroids in the presence of paramagnetic ions (i.e. Gd3 ) was recently demonstrated. However, Gd3 is relatively toxic at concentrations above 50 mM normally used to enable magnetic levitation with NdFeB-permanent magnets. Using a high magnetic field (a 50 mm-bore, 31 T Bitter magnet) at the High Field Magnet Laboratory at Radboud University in Nijmegen, The Netherlands, we performed magnetic levitational assembly of tissue constructs from living spheroids prepared from the SW1353 + chondrosarcoma cell line at 0.8 mM Gd3 containing salt gadobutrol at 19 T magnetic field. The parameters of the levitation process were determined on the basis of polystyrene beads with a 170 μm- diameter. To predict the theoretical possibility of assembly, a zone of stable levitation in the horizontal and vertical areas of cross sections was previously calculated. The construct from tissue spheroids partially fused after 3 h in levitation. The analysis of viability after prolonged exposure (1h) to strong magnetic fields (up to 30 T) showed the absence of significant cytotoxicity or morphology changes in the tissue spheroids. A high magnetic field works as a temporal and removal support or so-called ‘scaffield’. Thus, formative biofabrication of tissue-engineered constructs from tissue spheroids in the high magnetic field is a promising research direction 1. Introduction used successfully and broadly in different areas of technology and industries [3]. In 1997, Geim per- Since the early 1990s, several authors have demon- formed the diamagnetic levitation of a living organism strated the potential of levitation in air of water and (frog) in the air at the High Field Magnet Laboratory at other diamagnetic substances [1, 2]. Ikezoe et al have Radboud University in Nijmegen, The Netherlands, succeeded in levitating, in the atmosphere, a paramag- which was a breakthrough in the area of magnetic ( netic water ball containing CuSO4 they have named levitation [4]. In cell biology, as cells or tissue this phenomena ‘magneto-Archimedes levitation’); spheroids (cell aggregates) are considered to be although before this it was claimed that it should be diamagnetic, it has been proposed that their levitation impossible to levitate paramagnetic substances [2]. could be achieved by using a paramagnetic medium. Since then, principles of magnetic levitation are being The most commonly used paramagnetic agents are © 2020 IOP Publishing Ltd Biofabrication 12 (2020) 045022 V A Parfenov et al gadolinium (III) chelates. This approach implies the magnetic levitational bioassembly of tissue constructs creation of a 3D magnetic trap for diamagnetic objects in a high magnetic field. in an aqueous solution of paramagnetic ions. Winkle- Here, we report a first time successful magnetic man et al demonstrated trapping of polystyrene levitation bioassembly of 3D tissue constructs from spheres and of various types of living cells: the mouse tissue spheroids fabricated from the SW1353 chon- fibroblast cell line NIH-3T3, yeast (Saccharomyces drosarcoma cell line at 100 times lower, non-toxic cerevisiae), and algae (Chlamydomonas reinhardtii) concentration of a paramagnetic medium (aqueous using permanent magnets in the 40 mM paramagnetic gadolinium salt solution) in a high magnetic field. We gadolinium salt solution [5]. After studies of White- show the absence of any toxic effects of either the high sides’s group [6] and a series of publications from magnetic field or the low concentration of gadolinium Demirci’s group (both from Harvard University) on the viability of the cells and tissue constructs. Our [7–10] several research teams around the world also data demonstrate that magnetic levitational bioassem- demonstrated that a magnetic levitational bioassembly bly at a non-toxic concentration of gadolinium is tech- using a paramagnetic medium is technologically nologically feasible. Moreover, our experimental feasible [11, 12]. It is worth mentioning that this results confirmed the validity of proposals to use a approach avoids the use of ‘labels’ of any type, namely magnetic levitational bioassembly in a high magnetic magnetic nanoparticles which are cytotoxic and are field as a cost-effective alternative to microgravity proved to accumulate in human organisms after research at The International Space Station [18–20]. implantation of tissue-engineered constructs contain- We are convinced that the described methodological ing nanoparticles [13–15]. approach can be further used for systematic studies of Gadolinium(III) chelates are broadly used as con- the biological effects of microgravity on living objects trast agents which are approved by the FDA for appli- at high magnetic fields on Earth. cation in clinical imaging, such as MRI [16]. For our experiments we selected an FDA-approved + Gd3 -agent with known lowest possible toxicity— 2. Materials and methods gadobutrol (trade name ‘Gadovist’). However, the + high concentrations of Gd3 can be potentially toxic 2.1. Cell culture for cells and tissue spheroids, and a certain risk exists
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