AccScience Publishing / IJB / Online First / DOI: 10.36922/ijb.7888
Submit to IJB
Cite this article
135
Download
1240
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
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
Show Less
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
†These authors contributed equally to this work.
IJB 2025, 11(2), 448–473; 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/ )
Download PDF
Cite
XML
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.
References
  1. Timmis A, Townsend N, Gale CP, et al. European Society of Cardiology: Cardiovascular Disease Statistics 2019. Eur Heart J. Jan 1 2020;41(1):12-85. doi: 10.1093/eurheartj/ehz859
  2. Injury GBDTB, Spinal Cord Injury C. Global, regional, and national burden of traumatic brain injury and spinal cord injury, 1990-2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol. 2019;18(1):56-87. doi: 10.1016/S1474-4422(18)30415-0
  3. Tripathi S, Mandal SS, Bauri S, Maiti P. 3D bioprinting and its innovative approach for biomedical applications. MedComm (2020). 2023;4(1):e194. doi: 10.1002/mco2.194
  4. Zaszczynska A, Moczulska-Heljak M, Gradys A, Sajkiewicz P. Advances in 3D printing for tissue engineering. Materials (Basel). 2021;14(12):3149. doi: 10.3390/ma14123149
  5. Ng WL, Shkolnikov V. Jetting-based bioprinting: process, dispense physics, and applications. Bio-Des Manuf. 2024;7(5):771-799. doi: 10.1007/s42242-024-00285-3
  6. Li Y, Zhang X, Zhang X, Zhang Y, Hou D. Recent progress of the vat photopolymerization technique in tissue engineering: a brief review of mechanisms, methods, materials, and applications. Polymers (Basel). 2023;15(19):3940. doi: 10.3390/polym15193940
  7. Saini G, Segaran N, Mayer JL, Saini A, Albadawi H, Oklu R. Applications of 3D bioprinting in tissue engineering and regenerative medicine. J Clin Med. 2021;10(21):4966. doi: 10.3390/jcm10214966
  8. Liang K. Tissue bioprinting: promise and challenges. Bioengineering (Basel). 2023;10(12):1400. doi: 10.3390/bioengineering10121400
  9. Gomez-Florit M, Pardo A, Domingues RMA, et al. Natural-based hydrogels for tissue engineering applications. Molecules. 2020;25(24):5858. doi: 10.3390/molecules25245858
  10. Gyles DA, Castro LD, Silva JOC, Ribeiro-Costa RM. A review of the designs and prominent biomedical advances of natural and synthetic hydrogel formulations. Eur Polym J. 2017;88:373-392. doi: 10.1016/j.eurpolymj.2017.01.027
  11. García-García ÓD, Chato-Astrain J, Hochuli AHD, Pozzobon M, Carriel V. Decellularized tissue-derived materials for grafts development. In: Maia FRA, Oliveira JM, Reis RL. Handbook of the Extracellular Matrix. Cham: Springer; 2024:1011-1045:chap. 49. doi: 10.1007/978-3-030-92090-6_49-1
  12. Roche CD, Sharma P, Ashton AW, Jackson C, Xue M, Gentile C. Printability, durability, contractility and vascular network formation in 3D bioprinted cardiac endothelial cells using alginate-gelatin hydrogels. Front Bioeng Biotechnol. 2021;9:636257. doi: 10.3389/fbioe.2021.636257
  13. Moro A, Samanta S, Honkamaki L, et al. Hyaluronic acid based next generation bioink for 3D bioprinting of human stem cell derived corneal stromal model with innervation. Biofabrication. 2022;15(1):015020. doi: 10.1088/1758-5090/acab34
  14. Hewawasam RS, Blomberg R, Serbedzija P, Magin CM. Chemical modification of human decellularized extracellular matrix for incorporation into phototunable hybrid-hydrogel models of tissue fibrosis. ACS Appl Mater Interfaces. 2023;15(12):15071-15083. doi: 10.1021/acsami.2c18330
  15. Ndlovu SP, Ngece K, Alven S, Aderibigbe BA. Gelatin-based hybrid scaffolds: promising wound dressings. Polymers (Basel). 2021;13(17):2959. doi: 10.3390/polym13172959
  16. Lukin I, Erezuma I, Maeso L, et al. Progress in gelatin as biomaterial for tissue engineering. Pharmaceutics. 2022;14(6):1177. doi: 10.3390/pharmaceutics14061177
  17. Ribeiro AM, Meneses AC, Neumann IA. Polymeric nanoparticles and sponges in the control and stagnation of bleeding and wound healing. Desi Nanostruct Versatile Therap Appl. 2018;2018:189-219. doi: 10.1016/B978-0-12-813667-6.00005-X
  18. Wang X, Ao Q, Tian X, et al. Gelatin-Based Hydrogels for Organ 3D Bioprinting. Polymers (Basel). 2017; 9(9):401. doi: 10.3390/polym9090401
  19. Agten H, Van Hoven I, Van Hoorick J, Van Vlierberghe S, Luyten FP, Bloemen V. In vitro and in vivo evaluation of periosteum-derived cells and iPSC-derived chondrocytes encapsulated in GelMA for osteochondral tissue engineering. Front Bioeng Biotechnol. 2024; “12:1386692. doi: 10.3389/fbioe.2024.1386692
  20. Van Den Bulcke AI, Bogdanov B, De Rooze N, Schacht EH, Cornelissen M, Berghmans H. Structural and rheological properties of methacrylamide modified gelatin hydrogels. Biomacromolecules. 2000;1(1):31-38. doi: 10.1021/bm990017d
  21. Bedell ML, Torres AL, Hogan KJ, et al. Human gelatin-based composite hydrogels for osteochondral tissue engineering and their adaptation into bioinks for extrusion, inkjet, and digital light processing bioprinting. Biofabrication. 2022;14(4):10.1088/1758-5090/ac8768. doi: 10.1088/1758-5090/ac8768
  22. Lim KS, Klotz BJ, Lindberg GCJ, et al. Visible light cross-linking of gelatin hydrogels offers an enhanced cell microenvironment with improved light penetration depth. Macromol Biosci. 2019;19(6):e1900098. doi: 10.1002/mabi.201900098
  23. Koti P, Muselimyan N, Mirdamadi E, Asfour H, Sarvazyan NA. Use of GelMA for 3D printing of cardiac myocytes and fibroblasts. J 3D Print Med. 2019;3(1):11-22. doi: 10.2217/3dp-2018-0017
  24. Xu L, Zhang Z, Jorgensen AM, et al. Bioprinting a skin patch with dual-crosslinked gelatin (GelMA) and silk fibroin (SilMA): an approach to accelerating cutaneous wound healing. Mater Today Bio. 2023;18:100550. doi: 10.1016/j.mtbio.2023.100550
  25. Klotz BJ, Lim KS, Chang YX, et al. Engineering of a complex bone tissue model with endothelialised channels and capillary-like networks. Eur Cell Mater. 2018;35:335-348. doi: 10.22203/eCM.v035a23
  26. Hu C, Ahmad T, Haider MS, et al. A thermogelling organic-inorganic hybrid hydrogel with excellent printability, shape fidelity and cytocompatibility for 3D bioprinting. Biofabrication. 2022;14(2):025005. doi: 10.1088/1758-5090/ac40ee
  27. Liu S, Bernhardt A, Wirsig K, et al. Synergy of inorganic and organic inks in bioprinted tissue substitutes: Construct stability and cell response during long-term cultivation in vitro. Compos B: Eng. 2023;261:110804. doi: 10.1016/j.compositesb.2023.110804
  28. Fang X, Guo H, Zhang W, et al. Reduced graphene oxide- GelMA-PCL hybrid nanofibers for peripheral nerve regeneration. J Mater Chem B. 2020;8(46):10593-10601. doi: 10.1039/d0tb00779j
  29. Lopez-Gonzalez I, Zamora-Ledezma C, Sanchez-Lorencio MI, Tristante Barrenechea E, Gabaldon-Hernandez JA, Meseguer-Olmo L. Modifications in gene expression in the process of osteoblastic differentiation of multipotent bone marrow-derived human mesenchymal stem cells induced by a novel osteoinductive porous medical-grade 3D-printed poly(epsilon-caprolactone)/beta-tricalcium phosphate composite. Int J Mol Sci. 2021;22(20):11216. doi: 10.3390/ijms222011216
  30. Yaragalla S, Bhavitha KB, Athanassiou A. A review on graphene based materials and their antimicrobial properties. Coatings. 2021;11(10):1197. doi: 10.3390/coatings11101197
  31. Patil R, Alimperti S. Graphene in 3D bioprinting. J Funct Biomater. 2024;15(4):82. doi: 10.3390/jfb15040082
  32. Magne TM, de Oliveira Vieira T, Alencar LMR, et al. Graphene and its derivatives: understanding the main chemical and medicinal chemistry roles for biomedical applications. J Nanostructure Chem. 2022;12(5):693-727. doi: 10.1007/s40097-021-00444-3
  33. Kosowska K, Korycka P, Jankowska-Snopkiewicz K, et al. Graphene oxide (go)-based bioink with enhanced 3d printability and mechanical properties for tissue engineering applications. Nanomaterials (Basel). 2024;14(9):760. doi: 10.3390/nano14090760
  34. Vijayavenkataraman S, Thaharah S, Zhang S, Lu WF, Fuh JYH. 3D-printed PCL/rGO conductive scaffolds for peripheral nerve injury repair. Artif Organs. 2019;43(5):515-523. doi: 10.1111/aor.13360
  35. Magaz A, Li X, Gough JE, Blaker JJ. Graphene oxide and electroactive reduced graphene oxide-based composite fibrous scaffolds for engineering excitable nerve tissue. Mater Sci Eng C Mater Biol Appl. 2021;119:111632. doi: 10.1016/j.msec.2020.111632
  36. Saito N, Aoki K, Usui Y, et al. Application of carbon fibers to biomaterials: a new era of nano-level control of carbon fibers after 30-years of development. Chem Soc Rev. 2011;40(7):3824-3834. doi: 10.1039/c0cs00120a
  37. Mehrabi A, Baheiraei N, Adabi M, Amirkhani Z. Development of a novel electroactive cardiac patch based on carbon nanofibers and gelatin encouraging vascularization. Appl Biochem Biotechnol. 2020;190(3):931-948. doi: 10.1007/s12010-019-03135-6
  38. Salesa B, Assis M, Andres J, Serrano-Aroca A. Carbon nanofibers versus silver nanoparticles: time-dependent cytotoxicity, proliferation, and gene expression. Biomedicines. 2021;9(9):1155. doi: 10.3390/biomedicines9091155
  39. Rivera-Briso AL, Aachmann FL, Moreno-Manzano V, Serrano-Aroca A. Graphene oxide nanosheets versus carbon nanofibers: enhancement of physical and biological properties of poly(3-hydroxybutyrate-co-3- hydroxyvalerate) films for biomedical applications. Int J Biol Macromol. 2020;143:1000-1008. doi: 10.1016/j.ijbiomac.2019.10.034
  40. de Frutos S, Griera M, Lavín-Lopez MDP, et al. A new graphene-based nanomaterial increases lipolysis and reduces body weight gain through integrin linked kinase (ILK). Biomater Sci. 2023;11(14):4916-4929. doi: 10.1039/d2bm01791a
  41. Lavín-López MdP, Torres-Torresano M, García-Cuesta EM, et al. A graphene-based bioactive product with a non-immunological impact on mononuclear cell populations from healthy volunteers. Nanomaterials. 2024;14(23):1945. doi: 10.3390/nano14231945
  42. Etayo-Escanilla M, Campillo N, Avila-Fernandez P, et al. Comparison of printable biomaterials for use in neural tissue engineering: an in vitro characterization and in vivo biocompatibility assessment. Polymers (Basel). 2024;16(10):1426. doi: 10.3390/polym16101426
  43. Chato-Astrain J, Chato-Astrain I, Sanchez-Porras D, et al. Generation of a novel human dermal substitute functionalized with antibiotic-loaded nanostructured lipid carriers (NLCs) with antimicrobial properties for tissue engineering. J Nanobiotechnology. 2020;18(1):174. doi: 10.1186/s12951-020-00732-0
  44. Carriel V, Scionti G, Campos F, et al. In vitro characterization of a nanostructured fibrin agarose bio-artificial nerve substitute. J Tissue Eng Regen Med. 2017;11(5):1412-1426. doi: 10.1002/term.2039
  45. Gila-Vilchez C, Manas-Torres MC, Garcia-Garcia OD, et al. Biocompatible short-peptides fibrin co-assembled hydrogels. ACS Appl Polym Mater. 2023;5(3):2154-2165. doi: 10.1021/acsapm.2c02164
  46. Campos F, Bonhome-Espinosa AB, Vizcaino G, et al. Generation of genipin cross-linked fibrin-agarose hydrogel tissue-like models for tissue engineering applications. Biomed Mater. 2018;13(2):025021. doi: 10.1088/1748-605X/aa9ad2
  47. Chato-Astrain J, Campos F, Roda O, et al. In vivo evaluation of nanostructured fibrin-agarose hydrogels with mesenchymal stem cells for peripheral nerve repair. Front Cell Neurosci. 2018;12:501. doi: 10.3389/fncel.2018.00501
  48. Lotfy A, Salama M, Zahran F, Jones E, Badawy A, Sobh M. Characterization of mesenchymal stem cells derived from rat bone marrow and adipose tissue: a comparative study. Int J Stem Cells. 2014;7(2):135-142. doi: 10.15283/ijsc.2014.7.2.135
  49. Sun CK, Yen CH, Lin YC, et al. Autologous transplantation of adipose-derived mesenchymal stem cells markedly reduced acute ischemia-reperfusion lung injury in a rodent model. J Transl Med. 2011;9:118. doi: 10.1186/1479-5876-9-118
  50. Durand-Herrera D, Campos F, Jaimes-Parra BD, et al. Wharton’s jelly-derived mesenchymal cells as a new source for the generation of microtissues for tissue engineering applications. Histochem Cell Biol. 2018;150(4):379-393. doi: 10.1007/s00418-018-1685-6
  51. Sanchez-Porras D, Bermejo-Casares F, Carmona R, Weiss T, Campos F, Carriel V. Tissue fixation and processing for the histological identification of lipids. Methods Mol Biol. 2023;2566:175-186. doi: 10.1007/978-1-0716-2675-7_14
  52. Garcia-Garcia OD, El Soury M, Gonzalez-Quevedo D, et al. Histological, biomechanical, and biological properties of genipin-crosslinked decellularized peripheral nerves. Int J Mol Sci. 2021;22(2):674. doi: 10.3390/ijms22020674
  53. Geim AK, Novoselov KS. The rise of graphene. Nat Mater. 2007;6(3):183-191. doi: 10.1038/nmat1849
  54. Novoselov KS, Fal’ko VI, Colombo L, Gellert PR, Schwab MG, Kim K. A roadmap for graphene. Nature. 2012;490(7419):192-200. doi: 10.1038/nature11458
  55. Gu H, Tang H, Xiong P, Zhou Z. Biomarkers-based biosensing and bioimaging with graphene for cancer diagnosis. Nanomaterials (Basel). 2019;9(1):130. doi: 10.3390/nano9010130
  56. Li X, Chen A, Liu Y, Li L. Preparation and rectal administration of hydroxybutyl chitosan/graphene oxide composite thermosensitive hydrogel. React Funct Polym. 2023;189:105608. doi: 10.1016/j.reactfunctpolym.2023.105608
  57. Rajaei M, Rashedi H, Yazdian F, Navaei-Nigjeh M, Rahdar A, Díez-Pascual AM. Chitosan/agarose/graphene oxide nanohydrogel as drug delivery system of 5-fluorouracil in breast cancer therapy. J Drug Deliv Sci Technol. 2023;82:104307. doi: 10.1016/j.jddst.2023.104307
  58. Chen C, Xi Y, Weng Y. Progress in the development of graphene-based biomaterials for tissue engineering and regeneration. Materials (Basel). 2022;15(6):2164. doi: 10.3390/ma15062164
  59. de Carvalho JO, de Carvalho Oliveira F, Freitas SAP, et al. Carbon nanomaterials for treating osteoporotic vertebral fractures. Curr Osteoporos Rep. 2018;16(5):626-634. doi: 10.1007/s11914-018-0476-2
  60. Aparicio-Collado JL, Zheng Q, Molina-Mateo J, et al. Engineered highly porous polyvinyl alcohol hydrogels with poly(3-hydroxybutyrate-co-3-hydroxyvalerate) and graphene nanosheets for musculoskeletal tissue engineering: morphology, water sorption, thermal, mechanical, electrical properties, and biocompatibility. Materials (Basel). 2023;16(8):3114. doi: 10.3390/ma16083114
  61. Li A, Zhang C, Zhang YF. Thermal conductivity of graphene-polymer composites: mechanisms, properties, and applications. Polymers (Basel). 2017;9(9):437. doi: 10.3390/polym9090437
  62. Wu JB, Lin ML, Cong X, Liu HN, Tan PH. Raman spectroscopy of graphene-based materials and its applications in related devices. Chem Soc Rev. 2018;47(5):1822-1873. doi: 10.1039/c6cs00915h
  63. Sato Y, Shibata K, Kataoka H, et al. Strict preparation and evaluation of water-soluble hat-stacked carbon nanofibers for biomedical application and their high biocompatibility: influence of nanofiber-surface functional groups on cytotoxicity. Mol Biosyst. 2005;1(2):142-145. doi: 10.1039/b501222h
  64. Wang W, Junior JRP, Nalesso PRL, et al. Engineered 3D printed poly(varepsilon-caprolactone)/graphene scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl. 2019;100:759-770. doi: 10.1016/j.msec.2019.03.047
  65. Ferreras A, Matesanz A, Mendizabal J, et al. Light-responsive and antibacterial graphenic materials as a holistic approach to tissue engineering. ACS Nanosci Au. 2024;4(4):263-272. doi: 10.1021/acsnanoscienceau.4c00006
  66. Rivera-Briso AL, Aparicio-Collado JL, Serra RSI, Serrano- Aroca A. Graphene oxide versus carbon nanofibers in poly(3-hydroxybutyrate-co-3-hydroxyvalerate) films: degradation in simulated intestinal environments. Polymers (Basel). 2022;14(2):348. doi: 10.3390/polym14020348
  67. Lee WC, Lim CH, Shi H, et al. Origin of enhanced stem cell growth and differentiation on graphene and graphene oxide. ACS Nano. 2011;5(9):7334-7341. doi: 10.1021/nn202190c
  68. Murjani BO, Kadu PS, Bansod M, Vaidya SS, Yadav MD. Carbon nanotubes in biomedical applications: current status, promises, and challenges. Carbon Lett. 2022;32(5):1207-1226. doi: 10.1007/s42823-022-00364-4
  69. Shahazi R, Majumdar S, Saddam AI, Mondal J, Rahman MM, Alam MM. Carbon nanomaterials for biomedical applications: a comprehensive review. Nano Carbons. 2023;1(1):448. doi: 10.59400/n-c.v1i1.448
  70. Kalman J, Merino C, Fernandez-Cruz ML, Navas JM. Usefulness of fish cell lines for the initial characterization of toxicity and cellular fate of graphene-related materials (carbon nanofibers and graphene oxide). Chemosphere. 2019;218:347-358. doi: 10.1016/j.chemosphere.2018.11.130
  71. Shin SR, Zihlmann C, Akbari M, et al. Reduced graphene oxide-GelMA hybrid hydrogels as scaffolds for cardiac tissue engineering. Small. 2016;12(27):3677-3689. doi: 10.1002/smll.201600178
  72. Wei Z, Harris BT, Zhang LG. Gelatin methacrylamide hydrogel with graphene nanoplatelets for neural cell-laden 3D bioprinting. Annu Int Conf IEEE Eng Med Biol Soc. 2016;2016:4185-4188. doi: 10.1109/EMBC.2016.7591649
  73. Flachs D, Etzel J, Mayer M, et al. Characterization of electrically conductive, printable ink based on alginate hydrogel and graphene nanoplatelets. Biomed Eng Adv. 2022;4:100045. doi: 10.1016/j.bea.2022.100045
  74. Huang H-Y, Fan F-Y, Shen Y-K, et al. 3D poly-ε-caprolactone/ graphene porous scaffolds for bone tissue engineering. Colloids Surf A: Physicochem Eng Aspects. 2020;606:125393. doi: 10.1016/j.colsurfa.2020.125393
  75. Guimarães CF, Gasperini L, Marques AP, Reis RL. The stiffness of living tissues and its implications for tissue engineering. Nat Rev Mater. 2020;5(5):351-370. doi: 10.1038/s41578-019-0169-1
  76. Ahmed J, Mulla M, Maniruzzaman M. Rheological and dielectric behavior of 3D-printable chitosan/graphene oxide hydrogels. ACS Biomater Sci Eng. 2020;6(1):88-99. doi: 10.1021/acsbiomaterials.9b00201
  77. Li H, Liu S, Li L. Rheological study on 3D printability of alginate hydrogel and effect of graphene oxide. Int J Bioprint. 2024;2(2):54-66. doi: 10.18063/ijb.2016.02.007
  78. Bao Q, Zhang H, Yang Jx, et al. Graphene–polymer nanofiber membrane for ultrafast photonics. Adv Funct Mater. 2010;20(5):782-791. doi: 10.1002/adfm.200901658
  79. Wang X, Zhi L, Mullen K. Transparent, conductive graphene electrodes for dye-sensitized solar cells. Nano Lett. 2008;8(1):323-327. doi: 10.1021/nl072838r
  80. Galano A. Carbon nanotubes as free-radical scavengers. J Phys Chem C. 2008;112(24):8922-8927. doi: 10.1021/jp801379g
  81. Engstrom TA, Pogoda K, Cruz K, Janmey PA, Schwarz JM. Compression stiffening in biological tissues: On the possibility of classic elasticity origins. Phys Rev E. 2019;99(5-1):052413. doi: 10.1103/PhysRevE.99.052413
  82. Mishra A, Cleveland RO. Rheological properties of porcine organs: measurements and fractional viscoelastic model. Front Bioeng Biotechnol. 2024;12:1386955. doi: 10.3389/fbioe.2024.1386955
  83. Biggs LC, Kim CS, Miroshnikova YA, Wickstrom SA. Mechanical forces in the skin: roles in tissue architecture, stability, and function. J Invest Dermatol. 2020;140(2):284-290. doi: 10.1016/j.jid.2019.06.137
  84. Ma R, Wang Y, Qi H, et al. Nanocomposite sponges of sodium alginate/graphene oxide/polyvinyl alcohol as potential wound dressing: In vitro and in vivo evaluation. Compos Part B: Eng. 2019;167:396-405. doi: 10.1016/j.compositesb.2019.03.006
  85. Xu HQ, Liu JC, Zhang ZY, Xu CX. A review on cell damage, viability, and functionality during 3D bioprinting. Mil Med Res. 2022;9(1):70. doi: 10.1186/s40779-022-00429-5
  86. Middleton JC, Tipton AJ. Synthetic biodegradable polymers as orthopedic devices. Biomaterials. 2000;21(23): 2335-2346. doi: 10.1016/s0142-9612(00)00101-0
  87. Fournier E, Passirani C, Montero-Menei CN, Benoit JP. Biocompatibility of implantable synthetic polymeric drug carriers: focus on brain biocompatibility. Biomaterials. 2003;24(19):3311-3331. doi: 10.1016/s0142-9612(03)00161-3
  88. Nyska A, Schiffenbauer YS, Brami CT, Maronpot RR, Ramot Y. Histopathology of biodegradable polymers: challenges in interpretation and the use of a novel compact MRI for biocompatibility evaluation. Polym Adv Technol. 2014;25(5):461-467. doi: 10.1002/pat.3238
  89. Monteiro N, Thrivikraman G, Athirasala A, et al. Photopolymerization of cell-laden gelatin methacryloyl hydrogels using a dental curing light for regenerative dentistry. Dent Mater. 2018;34(3):389-399. doi: 10.1016/j.dental.2017.11.020
  90. Ding X, Pang Y, Liu Q, et al. GO-PEG represses the progression of liver inflammation via regulating the M1/M2 polarization of Kupffer cells. Small. 2024;20(26):e2306483. doi: 10.1002/smll.202306483
  91. Huaux F, d’Ursel de Bousies V, Parent MA, et al. Mesothelioma response to carbon nanotubes is associated with an early and selective accumulation of immunosuppressive monocytic cells. Part Fibre Toxicol. 2016;13(1):46. doi: 10.1186/s12989-016-0158-0
  92. Zhang X, Luo M, Zhang J, et al. Carbon nanotubes promote alveolar macrophages toward M2 polarization mediated epithelial-mesenchymal transition and fibroblast-to-myofibroblast transdifferentiation. Nanotoxicology. 2021;15(5):588-604. doi: 10.1080/17435390.2021.1905098
  93. Zarrintaj P, Manouchehri S, Ahmadi Z, et al. Agarose-based biomaterials for tissue engineering. Carbohydr Polym. 2018;187:66-84. doi: 10.1016/j.carbpol.2018.01.060
  94. Koffler J, Zhu W, Qu X, et al. Biomimetic 3D-printed scaffolds for spinal cord injury repair. Nat Med. 2019;25(2): 263-269. doi: 10.1038/s41591-018-0296-z

 

 

 

 

 

Share
Back to top
International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
We use cookies on our website to ensure you get the best experience.
Read more about our cookies here
Accept