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RESEARCH ARTICLE

Development and characterization of graphene derivative–GelMA hybrid bioinks for the generation of bioartificial tissue substitutes via 3D bioprinting

María del Prado Lavín-López1† ,  Óscar Darío García-García2† ,  Fernanda Condi de Godoi3 ,  Mercedes Griera-Merino4 ,  Ignasi Jorba5 ,  Fernando Campos2 ,  Sergio de Frutos6 ,  Iván López-González7* ,  José Manuel Baena7,8 ,  Víctor Carriel2* ,  Noelia Campillo7,8
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1 Graphenano S.L., Murcia, Spain
2 Tissue Engineering Group, Department of Histology, University of Granada and Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain
3 Tessenderlo Innovation Center and PB Leiner, Tessenderlo Group nv, Brussels, Belgium
4 Graphenano Medical Care S.L., Madrid, Spain
5 Unit of Biophysics and Bioengineering, School of Medicine, University of Barcelona, Barcelona, Spain
6 Unit of Physiology, Department of Systems Biology, School of Medicine, University of Alcalá, Madrid, Spain
7 REGEMAT 3D S.L., Granada, Spain
8 BRECA Health Care S.L., Granada, Spain
IJB, 7888 https://doi.org/10.36922/ijb.7888
Submitted: 17 December 2024 | Accepted: 5 February 2025 | Published: 6 February 2025
(This article belongs to the Special Issue Bioprinting of in Vitro Tissue and Disease Models)
© 2025 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

The fabrication of bioartificial tissue substitutes is a complex process that relies on the application of innovative biomaterials and manufacturing techniques enabling the generation of cell-laden scaffolds mimicking natural tissue interfaces. Among the many biomaterials, gelatin methacryloyl (GelMA) hydrogels have shown great potential for three-dimensional (3D) bioprinting-based tissue engineering due to their high biocompatibility, biodegradability, and tunable mechanical properties. In this study, the potential use of hybrid hydrogels based on GelMA and a highly purified graphene-derivative (BioGraph) as biomaterials bioinks for extrusion-based 3D bioprinting was investigated. Formulations containing BioGraph concentrations of up to 0.1% w/v were well-suited for this technique, showing good extrudability with reduced clogging at the printing temperatures, effective photocrosslinking at the irradiances tested, high shape fidelity, and high resolution of the printed scaffold. In situ photocrosslinking tests revealed that BioGraph concentration decreased the speed of the photocrosslinking and the stiffness of the cured matrix. In vitro studies indicated that BioGraph content ≤0.1% w/v did not have an adverse impact on the viability and proliferation of rat adipose-derived mesenchymal stem cells (r-AMSCs). Similarly, acellular scaffolds implanted subcutaneously in rats showed a local macrophage-mediated inflammatory reaction and a collagen encapsulation process without any affection of surrounded host tissues. The addition of lower concentrations of BioGraph (0.025% w/v) to the matrix resulted in enhanced macrophagic interactions and scaffold degradation in vivo, and r-AMSCs growth and proliferation in vitro. In conclusion, the GelMA–BioGraph hybrid hydrogels developed here demonstrate enhanced rheological and biological properties, tailored for extrusion-based 3D bioprinting with applications in the engineering of soft (neural, liver, etc.) or hard (bone) tissues.

Graphical abstract
Keywords
3D bioprinting
Bioinks
Cell–biomaterial interactions
GelMA
Graphene
In vivo biocompatibility
Tissue engineering
Funding
The study was financed by the Spanish “Plan Estatal de Investigación Científica y Técnica y de Innovación 2021–2023, Proyectos de Colaboración Público-Privada, Ministerio de Ciencia e Innovación” (Grant No. CPP2021- 009070) and the “Plan Nacional de Investigación Científica, Desarrollo e Innovación Tecnológica, Ministerio de Economía y Competitividad (Instituto de Salud Carlos III)” (Grants No. FIS P23/00337, PI23/01071, and RD24/0004/0020). It was also co-funded by grant art.60 LOSU 2022/2024 from Universidad de Alcalá, Spain. N.C. was financed by Torres Quevedo Grant PTQ2019-010731 from Agencia Estatal de Investigación (10.13039/501100011033). I.J. was financed by the Beatriu de Pinós Program (Agència de Gestió d’Ajuts Universitaris i de Recerca, Generalitat de Catalunya; Grant BP 2021 00106).
Conflict of interest
F.C.G. declares that she is coinventor of the patent with code WO2020201555A1, named “A gelatin and uses thereof ” and that she worked for PB Leiner from 2018 to 2023, a company distributing Claro® BG800 product. M.P.L., M.G. and S.F. declare that they are coinventors of the patent with code WO/2020/016319, named “Graphene Product and Cosmetic Uses Thereof.” M.G. and M.P.L. are employed by the patent owners Graphenano or Graphenano Medical Care companies. J.M.B. declares that he is cofounder of REGEMAT 3D, a company distributing the REG4Life bioprinter used in this study. I.L. and N.C. declare that they currently or have previously worked for REGEMAT 3D, respectively. The above-mentioned authors declare that their contribution to this work and manuscript was made independently, without requirements or guidance from any employers. No financial compensation was received for the contributions made to this scientific work. The rest of authors declare no conflicts of interest.
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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
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