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RESEARCH ARTICLE

Nanomaterial-modified bioinks for DLP-based bioprinting of bone constructs: Impact on mechanical properties and mesenchymal stem cell function

Julie Kühl1 ,  Sven Malte Krümpelmann1 ,  Larissa Hildebrandt1 ,  Malte Bruhn2 ,  Jan-Bernd Hövener3 ,  Ronald Seidel3 ,  Stanislav Gorb4 ,  Fabian Schütt2 ,  Rainer Adelung2 ,  Andreas Seekamp1 ,  Leonard Siebert2 ,  Sabine Fuchs1*
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1 Experimental Trauma Surgery, Department of Orthopedics and Trauma Surgery, University Medical Center, Kiel, Germany
2 Functional Nanomaterials Group, Department of Materials Science, Faculty of Engineering, Kiel University, Kiel, Germany
3 Section for Biomedical Imaging (SBMI), Molecular Imaging North Competence Center (MOIN CC), Department of Radiology and Neuroradiology, University Medical Center Kiel, Kiel University, Kiel, Germany
4 Department of Functional Morphology and Biomechanics, Faculty of Mathematics and Natural Sciences, Kiel University, Kiel, Germany
IJB, 4015 https://doi.org/10.36922/ijb.4015
Submitted: 21 June 2024 | Accepted: 31 July 2024 | Published: 1 August 2024
(This article belongs to the Special Issue Bioprinting for Tissue Engineering and Modeling)
© 2024 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

3D printing technologies offer tremendous potential to produce patient-specific implants and treat critical-sized bone defects, which vary in size, shape, and clinical requirements. Despite advancements in 3D printing of biomaterial-based bone constructs, they often lack biologically active material. For larger-sized bone implants, early biologization and vascularization are essential. In this context, bioprinting technologies enable the integration of vital cells or active growth factors into 3D-printed constructs, while the integration of nanomaterials enables material-mediated functionalization of the bioink. To date, such bioink modifications with nanomaterials have rarely been reported for digital light processing (DLP) bioprinting technology. Furthermore, there is a notable lack of direct comparative studies on the impact of nanomaterials on cellular processes. In this study, we assessed and compared graphene oxide (GO)- and calcium phosphate (CaP)-modified bioinks for DLP bioprinting of methacrylated gelatin (GelMa)-based bone constructs. After printing, the impact of bioinks on cell distribution, viability, cell proliferation, and differentiation, as well as the mechanical and structural properties of constructs, was evaluated. In comparison to commercial bioinks, cell viability was higher in the established GelMa bioinks. Morphological data and DNA quantification indicate the highest cell vitality and proliferation over time in basic GelMa bioink. CaP-modified GelMa bioink displayed the highest differentiation of human mesenchymal stem cells (hMSCs), in terms of osteogenic gene expression and calcium deposition. Conversely, GO increased the Young’s modulus of the material, affecting cell morphology. Overall, the direct comparison of nanomaterials suggests diverse effects in functionalizing DLP-printed bone constructs containing living osteogenic cells.

Keywords
Hydrogel
Bone implant
Calcium phosphate
Graphene oxide
3D printing
GelMa
Nanomaterials
Bioprinting
Funding
This work was supported by the Federal Ministry of Education and Research (BMBF), Germany, through the WIR! program for BlueHealthTech and BlueBioPol (FKZ 03WIR6207A.BMBF). MOIN CC was founded by a grant from the European Regional Development Fund (ERDF) and the Zukunftsprogramm Wirtschaft of Schleswig- Holstein (project no. 122-09-053).
Conflict of interest
The authors declare they have no competing interests.
References
  1. Maruyama M, Rhee C, Utsunomiya T, et al. Modulation of the inflammatory response and bone healingr Review. Front Endocrinol. 2020;11:386. doi: 10.3389/fendo.2020.00386
  2. Ko HF, Sfeir C, Kumta PN. Novel synthesis strategies for natural polymer and composite biomaterials as potential scaffolds for tissue engineering. Philos Trans A Math Phys Eng Sci. 2010;368(1917):1981-1997. doi: 10.1098/rsta.2010.0009
  3. LeGeros RZ. Properties of osteoconductive biomaterials: calcium phosphates. Clin Orthop Relat Res. 2002;395:81-98. doi: 10.1097/00003086-200202000-00009
  4. Dimitriou R, Mataliotakis GI, Angoules AG, Kanakaris NK, Giannoudis PV. Complications following autologous bone graft harvesting from the iliac crest and using the RIA: a systematic review. Injury. 2011;42:S3-S15. doi: 10.1016/j.injury.2011.06.015
  5. Nauth A, Schemitsch E, Norris B, Nollin Z, Watson JT. Critical-size bone defects: is there a consensus for diagnosis and treatment? J Orthop Trauma. 2018;32(Suppl 1):S7-S11. doi: 10.1097/bot.0000000000001115
  6. Aktuglu K, Erol K, Vahabi A. Ilizarov bone transport and treatment of critical-sized tibial bone defects: a narrative review. J Orthop Traumatol. 2019;20(1):22. doi: 10.1186/s10195-019-0527-1
  7. Zhu W, Ma X, Gou M, Mei D, Zhang K, Chen S. 3D printing of functional biomaterials for tissue engineering. Curr Opin Biotechnol. 2016;40:103-112. doi: 10.1016/j.copbio.2016.03.014
  8. Haglin JM, Eltorai AE, Gil JA, Marcaccio SE, Botero- Hincapie J, Daniels AH. Patient-specific orthopaedic implants. Orthop Surg. 2016;8(4):417-424. doi: 10.1111/os.12282
  9. Mobbs RJ, Parr WCH, Huang C, Amin T. Rapid personalised virtual planning and on-demand surgery for acute spinal trauma using 3D-printing, biomodelling and patient-specific implant manufacture. J Pers Med. 2022; 12(6):997. doi: 10.3390/jpm12060997
  10. Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials. 2016;76:321-343. doi: 10.1016/j.biomaterials.2015.10.076
  11. Liang R, Gu Y, Wu Y, Bunpetch V, Zhang S. Lithography-based 3D bioprinting and bioinks for bone repair and regeneration. ACS Biomater Sci Eng. 2021;7(3): 806-816. doi: 10.1021/acsbiomaterials.9b01818
  12. Kim SH, Kim DY, Lim TH, Park CH. Silk fibroin bioinks for digital light processing (DLP) 3D bioprinting. Adv Exp Med Biol. 2020;1249:53-66. doi: 10.1007/978-981-15-3258-0_4
  13. Shen Y, Tang H, Huang X, et al. DLP printing photocurable chitosan to build bio-constructs for tissue engineering. Carbohydr Polym. 2020;235:115970. doi: 10.1016/j.carbpol.2020.115970
  14. Sheng L, Li M, Zheng S, Qi J. Adjusting the accuracy of PEGDA-GelMA vascular network by dark pigments via digital light processing printing. J. Biomater Appl. 2022;36(7):1173-1187. doi: 10.1177/08853282211053081
  15. Song P, Gui X, Wu L, et al. DLP fabrication of multiple hierarchical biomimetic GelMA/SilMA/HAp scaffolds for enhancing bone regeneration. Biomacromolecules. 2024;25(3):1871-1886. doi: 10.1021/acs.biomac.3c01318
  16. Tao J, Zhu S, Liao X, et al. DLP-based bioprinting of void-forming hydrogels for enhanced stem-cell-mediated bone regeneration. Mater Today Bio. 2022;17:100487. doi: 10.1016/j.mtbio.2022.100487
  17. Park SH, Park DS, Shin JW, et al. Scaffolds for bone tissue engineering fabricated from two different materials by the rapid prototyping technique: PCL versus PLGA. J Mater Sci Mater Med. 2012;23(11):2671-2678. doi: 10.1007/s10856-012-4738-8
  18. Tibbitt MW, Rodell CB, Burdick JA, Anseth KS. Progress in material design for biomedical applications. Proc Natl Acad Sci. 2015;112(47):14444-14451. doi: 10.1073/pnas.1516247112
  19. Nguyen DG, Funk J, Robbins JB, et al. Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. Plos One. 2016;11(7):e0158674. doi: 10.1371/journal.pone.0158674
  20. Lee KY, Mooney DJ. Hydrogels for tissue engineering. Chem Rev. 2001;101(7):1869-1880. doi: 10.1021/cr000108x
  21. Levato R, Visser J, Planell JA, Engel E, Malda J, Mateos- Timoneda MA. Biofabrication of tissue constructs by 3D bioprinting of cell-laden microcarriers. Biofabrication. 2014;6(3):035020. doi: 10.1088/1758-5082/6/3/035020
  22. Leijten J, Rouwkema J, Zhang YS, Nasajpour A, Dokmeci MR, Khademhosseini A. Advancing tissue engineering: a tale of nano-, micro-, and macroscale integration. Small. 2016;12(16):2130-2145. doi: 10.1002/smll.201501798
  23. Wüst S, Müller R, Hofmann S. Controlled positioning of cells in biomaterials—approaches towards 3D tissue printing. J Funct Biomater. 2011;2(3):119-154. doi: 10.3390/jfb2030119
  24. Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773-785. doi: 10.1038/nbt.2958
  25. Liu Y, Chan-Park MB. A biomimetic hydrogel based on methacrylated dextran-graft-lysine and gelatin for 3D smooth muscle cell culture. Biomaterials. 2010;31(6):1158-1170. doi: 10.1016/j.biomaterials.2009.10.040
  26. Jeong HJ, Nam H, Jang J, Lee SJ. 3D Bioprinting strategies for the regeneration of functional tubular tissues and organs. Bioengineering (Basel). 2020;7(2):32. doi: 10.3390/bioengineering7020032
  27. Xu T, Zhao W, Zhu J-M, Albanna MZ, Yoo JJ, Atala A. Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials. 2013;34(1):130-139. doi: 10.1016/j.biomaterials.2012.09.035
  28. Li J, Mooney DJ. Designing hydrogels for controlled drug delivery. Nat Rev Mater. 2016;1(12):16071. doi: 10.1038/natrevmats.2016.71
  29. Gao J, Li M, Cheng J, et al. 3D-printed GelMA/PEGDA/ F127DA scaffolds for bone regeneration. J Funct Biomater. 2023;14(2):96. doi: 10.3390/jfb14020096
  30. Gao J, Wang H, Li M, et al. DLP-printed GelMA-PMAA scaffold for bone regeneration through endochondral ossification. Int J Bioprint. 2023;9(5):754. doi: 10.18063/ijb.754
  31. Shi H, Li Y, Xu K, Yin J. Advantages of photo-curable collagen-based cell-laden bioinks compared to methacrylated gelatin (GelMA) in digital light processing (DLP) and extrusion bioprinting. Mater Today Bio. 2023;23:100799. doi: 10.1016/j.mtbio.2023.100799
  32. Kurian AG, Singh RK, Patel KD, Lee JH, Kim HW. Multifunctional GelMA platforms with nanomaterials for advanced tissue therapeutics. Bioact Mater. 2022;8: 267-295. doi: 10.1016/j.bioactmat.2021.06.027
  33. Li J, Moeinzadeh S, Kim C, et al. Development and systematic characterization of GelMA/alginate/PEGDMA/xanthan gum hydrogel bioink system for extrusion bioprinting. Biomaterials. 2023;293:121969. doi: 10.1016/j.biomaterials.2022.121969
  34. Pérez-Cortez JE, Sánchez-Rodríguez VH, Gallegos- Martínez S, et al. Low-cost light-based GelMA 3D bioprinting via retrofitting: manufacturability test and cell culture assessment. Micromachines (Basel). 2022; 14(1):55. doi: 10.3390/mi14010055
  35. Sun X, Ma Z, Zhao X, et al. Three-dimensional bioprinting of multicell-laden scaffolds containing bone morphogenic protein-4 for promoting M2 macrophage polarization and accelerating bone defect repair in diabetes mellitus. Bioact Mater. 2021;6(3):757-769. doi: 10.1016/j.bioactmat.2020.08.030
  36. Yi S, Liu Q, Luo Z, et al. Micropore-forming gelatin methacryloyl (GelMA) bioink toolbox 2.0: designable tunability and adaptability for 3D bioprinting applications. Small. 2022;18(25):e2106357. doi: 10.1002/smll.202106357
  37. Billiet T, Gevaert E, De Schryver T, Cornelissen M, Dubruel P. The 3D printing of gelatin methacrylamide cell-laden tissue-engineered constructs with high cell viability. Biomaterials. 2014;35(1):49-62. doi: 10.1016/j.biomaterials.2013.09.078
  38. Hospodiuk M, Dey M, Sosnoski D, Ozbolat IT. The bioink: a comprehensive review on bioprintable materials. Biotechnol Adv. 2017;35(2):217-239. doi: 10.1016/j.biotechadv.2016.12.006
  39. Gopinathan J, Noh I. Recent trends in bioinks for 3D printing. Biomater Res. 2018/04/06 2018;22(1):11. doi: 10.1186/s40824-018-0122-1
  40. Jammalamadaka U, Tappa K. Recent advances in biomaterials for 3D printing and tissue engineering. J Funct Biomater. 2018;9(1):22. doi: 10.3390/jfb9010022
  41. Huh J, Moon YW, Park J, Atala A, Yoo JJ, Lee SJ. Combinations of photoinitiator and UV absorber for cell-based digital light processing (DLP) bioprinting. Biofabrication. 2021;13(3): 034103. doi: 10.1088/1758-5090/abfd7a
  42. Peng X, Liu X, Yang Y, et al. Graphene oxide functionalized gelatin methacryloyl microgel for enhanced biomimetic mineralization and in situ bone repair. Int J Nanomedicine. 2023;18:6725-6741. doi: 10.2147/ijn.S433624
  43. Dinescu S, Ionita M, Ignat SR, Costache M, Hermenean A. Graphene oxide enhances chitosan-based 3D scaffold properties for bone tissue engineering. Int J Mol Sci. 2019;20(20):5077. doi: 10.3390/ijms20205077
  44. Li J, Liu X, Crook JM, Wallace GG. Development of 3D printable graphene oxide based bio-ink for cell support and tissue engineering. Front Bioeng Biotechnol. 2022;10:994776. doi: 10.3389/fbioe.2022.994776
  45. Wang C, Mallela J, Garapati US, et al. A chitosan-modified graphene nanogel for noninvasive controlled drug release. Nanomed Nanotechnol Biol Med. 2013;9(7):903-911. doi: 10.1016/j.nano.2013.01.003
  46. Zhang L, Li X, Shi C, et al. Biocompatibility and angiogenic effect of chitosan/graphene oxide hydrogel scaffolds on EPCs. Stem Cells International. 2021;2021:5594370. doi: 10.1155/2021/5594370
  47. Zhihui K, Min D. Application of graphene oxide-based hydrogels in bone tissue engineering. ACS Biomater Sci Eng. 2022;8(7):2849-2857. doi: 10.1021/acsbiomaterials.2c00396
  48. Zhou C, Liu S, Li J, et al. Collagen functionalized with graphene oxide enhanced biomimetic mineralization and in situ bone defect repair. ACS Appl Mater Interfaces. 2018;10(50):44080-44091. doi: 10.1021/acsami.8b17636
  49. Jeong J-T, Choi M-K, Sim Y, et al. Effect of graphene oxide ratio on the cell adhesion and growth behavior on a graphene oxide-coated silicon substrate. Sci Rep. 2016;6(1):33835. doi: 10.1038/srep33835
  50. Choe G, Oh S, Seok JM, Park SA, Lee JY. Graphene oxide/ alginate composites as novel bioinks for three-dimensional mesenchymal stem cell printing and bone regeneration applications. Nanoscale. 2019;11(48):23275-23285. doi: 10.1039/C9NR07643C
  51. Schmidleithner C, Malferrari S, Palgrave R, Bomze D, Schwentenwein M, Kalaskar DM. Application of high resolution DLP stereolithography for fabrication of tricalcium phosphate scaffolds for bone regeneration. Biomed Mater. 2019;14(4):045018. doi: 10.1088/1748-605X/ab279d
  52. Bhattacharyya A, Janarthanan G, Kim T, et al. Modulation of bioactive calcium phosphate micro/nanoparticle size and shape during in situ synthesis of photo-crosslinkable gelatin methacryloyl based nanocomposite hydrogels for 3D bioprinting and tissue engineering. Biomater Res. 2022;26(1):54. doi: 10.1186/s40824-022-00301-6
  53. Choi JB, Kim YK, Byeon SM, et al. Fabrication and characterization of biodegradable gelatin methacrylate/ biphasic calcium phosphate composite hydrogel for bone tissue engineering. Nanomaterials (Basel). 2021;11(3):617. doi: 10.3390/nano11030617
  54. Lee DN, Park JY, Seo YW, et al. Photo-crosslinked gelatin methacryloyl hydrogel strengthened with calcium phosphate-based nanoparticles for early healing of rabbit calvarial defects. J Periodontal Implant Sci. 2023;53(5):321-335. doi: 10.5051/jpis.2203220161
  55. Ren-Jie X, Jin-Jin M, Yu X, et al. A biphasic calcium phosphate/acylated methacrylate gelatin composite hydrogel promotes osteogenesis and bone repair. Connect Tissue Res. 2023;64(5):445-456. doi: 10.1080/03008207.2023.2212067
  56. Zhang X, Zhang H, Zhang Y, et al. 3D printed reduced graphene oxide-GelMA hybrid hydrogel scaffolds for potential neuralized bone regeneration. J Mater Chem B. 2023;11(6):1288-1301. doi: 10.1039/D2TB01979E
  57. Khan MUA, Razak SIA, Rehman S, Hasan A, Qureshi S, Stojanovic GM. Bioactive scaffold (sodium alginate)-g- (nHAp@SiO(2)@GO) for bone tissue engineering. Int J Biol Macromol. 2022;222(Pt A):462-472. doi: 10.1016/j.ijbiomac.2022.09.153
  58. Qi F, Wang C, Peng S, Shuai C, Yang W, Zhao Z. A co-dispersed nanosystem of strontium-anchored reduced graphene oxide to enhance the bioactivity and mechanical property of polymer scaffolds. Mater Chem Front. 2021;5(5): 2373-2386. doi: 10.1039/D0QM00958J
  59. Shuai C, Guo W, Wu P, et al. A graphene oxide-Ag co-dispersing nanosystem: dual synergistic effects on antibacterial activities and mechanical properties of polymer scaffolds. Chem Eng J. 2018;347:322-333. doi: 10.1016/j.cej.2018.04.092
  60. 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
  61. Vallet-Regí M, González-Calbet JM. Calcium phosphates as substitution of bone tissues. Progress in Solid State Chemistry. 2004;32(1):1-31. doi: 10.1016/j.progsolidstchem.2004.07.001
  62. Zhou B, Jiang X, Zhou X, et al. GelMA-based bioactive hydrogel scaffolds with multiple bone defect repair functions: therapeutic strategies and recent advances. Biomater Res. 2023;27(1):86. doi: 10.1186/s40824-023-00422-6
  63. Ginebra M-P, Espanol M, Maazouz Y, Bergez V, Pastorino D. Bioceramics and bone healing. EFORT Open Rev. 2018;3(5):173-183. doi: 10.1302/2058-5241.3.170056
  64. Alvarez K, Nakajima H. Metallic scaffolds for bone regeneration. Materials. 2009;2(3):790-832. doi: 10.3390/ma2030790
  65. Kühl J, Gorb S, Kern M, et al. Extrusion-based 3D printing of osteoinductive scaffolds with a spongiosa-inspired structure. Front Bioeng Biotechnol. 2023;11:1268049. doi: 10.3389/fbioe.2023.1268049
  66. Wang F, Saure LM, Schütt F, et al. Graphene oxide framework structures and coatings: impact on cell adhesion and pre-vascularization processes for bone grafts. Int J Mol Sci. 2022;23(6):3379. doi: 10.3390/ijms23063379
  67. Kolbe M, Xiang Z, Dohle E, Tonak M, Kirkpatrick CJ, Fuchs S. Paracrine effects influenced by cell culture medium and consequences on microvessel-like structures in cocultures of mesenchymal stem cells and outgrowth endothelial cells. Tissue Eng A. 2011;17(17–18):2199-2212. doi: 10.1089/ten.TEA.2010.0474
  68. Fuchs S, Hermanns MI, Kirkpatrick CJ. Retention of a differentiated endothelial phenotype by outgrowth endothelial cells isolated from human peripheral blood and expanded in long-term cultures. Cell Tissue Res. 2006;326:79-92. doi: 10.1007/s00441-006-0222-4
  69. Yue K, Trujillo-de Santiago G, Alvarez MM, Tamayol A, Annabi N, Khademhosseini A. Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels. Biomaterials. 2015;73:254-271. doi: 10.1016/j.biomaterials.2015.08.045
  70. Fedorov A, Beichel R, Kalpathy-Cramer J, et al. 3D slicer as an image computing platform for the quantitative imaging network. Magn Reson Imaging. 2012;30(9):1323-1341. doi: 10.1016/j.mri.2012.05.001
  71. Cignoni P, Callieri M, Corsini M, Dellepiane M, Ganovelli F, Ranzuglia G. MeshLab: an Open-Source Mesh Processing Tool. The Eurographics Association. 2008; 129-136. doi : 10.2312/LocalChapterEvents/ItalChap/ItalianChapConf2008/129-136
  72. Choi CE, Chakraborty A, Adzija H, et al. Metal organic framework-incorporated three-dimensional (3D) bio-printable hydrogels to facilitate bone repair: preparation and in vitro bioactivity analysis. Gels. 2023;9(12):923. doi: 10.3390/gels9120923
  73. Hildebrand T, Laib A, Müller R, Dequeker J, Rüegsegger P. Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res. 1999;14(7):1167-1174. doi: 10.1359/jbmr.1999.14.7.1167
  74. Doktor T, Valach J, Kytyr D, Jiroušek O. Pore Size Distribution of Human Trabecular Bone – Comparison of Intrusion Measurements with Image Analysis. 2011:115-118.
  75. Lim TC, Chian KS, Leong KF. Cryogenic prototyping of chitosan scaffolds with controlled micro and macro architecture and their effect on in vivo neo-vascularization and cellular infiltration. J Biomed Mater Res A. 2010;94A(4):1303-1311. doi: 10.1002/jbm.a.32747
  76. Zhou K, Yu P, Shi X, et al. Hierarchically porous hydroxyapatite hybrid scaffold incorporated with reduced graphene oxide for rapid bone ingrowth and repair. ACS Nano. 2019;13(8):9595-9606. doi: 10.1021/acsnano.9b04723
  77. Taniguchi N, Fujibayashi S, Takemoto M, et al. Effect of pore size on bone ingrowth into porous titanium implants fabricated by additive manufacturing: an in vivo experiment. Mater Sci Eng C. 2016;59:690-701. doi: 10.1016/j.msec.2015.10.069
  78. Xia P, Luo Y. Vascularization in tissue engineering: the architecture cues of pores in scaffolds. J Biomed Mater Res B Appl Biomater. 2022;110(5):1206-1214. doi: 10.1002/jbm.b.34979
  79. Abdollahiyan P, Oroojalian F, Mokhtarzadeh A, de la Guardia M. Hydrogel-Based 3D Bioprinting for bone and cartilage tissue engineering. Biotechnol J. 2020;15(12):e2000095. doi: 10.1002/biot.202000095
  80. de Leeuw AM, Graf R, Lim PJ, et al. Physiological cell bioprinting density in human bone-derived cell-laden scaffolds enhances matrix mineralization rate and stiffness under dynamic loading. Original research. Front Bioeng Biotechnol. 2024;12:1310289. doi: 10.3389/fbioe.2024.1310289
  81. Dhawan A, Kennedy PM, Rizk EB, Ozbolat IT. Three-dimensional bioprinting for bone and cartilage restoration in orthopaedic surgery. J Am Acad Orthop Surg. 2019;27(5):e215-e226. doi: 10.5435/jaaos-d-17-00632
  82. Midha S, Dalela M, Sybil D, Patra P, Mohanty S. Advances in three-dimensional bioprinting of bone: progress and challenges. J Tissue Eng Regen Med. 2019;13(6):925-945. doi: 10.1002/term.2847
  83. Zhang J, Eyisoylu H, Qin X-H, Rubert M, Müller R. 3D bioprinting of graphene oxide-incorporated cell-laden bone mimicking scaffolds for promoting scaffold fidelity, osteogenic differentiation and mineralization. Acta Biomaterialia. 2021;121:637-652. doi: 10.1016/j.actbio.2020.12.026
  84. Chen YC, Lin RZ, Qi H, et al. Functional human vascular network generated in photocrosslinkable gelatin methacrylate hydrogels. Adv Funct Mater. 2012;22(10):2027-2039. doi: 10.1002/adfm.201101662
  85. Tigner TJ, Rajput S, Gaharwar AK, Alge DL. Comparison of photo cross linkable gelatin derivatives and initiators for three-dimensional extrusion bioprinting. Biomacromolecules. 2020;21(2):454-463. doi: 10.1021/acs.biomac.9b01204
  86. Im G-B, Lin R-Z. Bioengineering for vascularization: trends and directions of photocrosslinkable gelatin methacrylate hydrogels. Review. Front Bioeng Biotechnol. 2022;10: 1053491. doi: 10.3389/fbioe.2022.1053491
  87. 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
  88. Kim J, Raja N, Choi YJ, et al. Enhancement of properties of a cell-laden GelMA hydrogel-based bioink via calcium phosphate phase transition. Biofabrication. 2023;16(1):ad05e2. doi: 10.1088/1758-5090/ad05e2
  89. Montelongo SA, Chiou G, Ong JL, Bizios R, Guda T. Development of bioinks for 3D printing microporous, sintered calcium phosphate scaffolds. J Mater Sci Mater Med. 2021;32(8):94. doi: 10.1007/s10856-021-06569-9
  90. Fischetti T, Borciani G, Avnet S, et al. Incorporation/ enrichment of 3D bioprinted constructs by biomimetic nanoparticles: tuning printability and cell behavior in bone models. Nanomaterials (Basel). 2023;13(14):2040. doi: 10.3390/nano13142040
  91. Raghav PK, Mann Z, Ahlawat S, Mohanty S. Mesenchymal stem cell-based nanoparticles and scaffolds in regenerative medicine. Eur J Pharmacol. 2022;918:174657. doi: 10.1016/j.ejphar.2021.174657
  92. Cernencu AI, Vlasceanu GM, Serafim A, Pircalabioru G, Ionita M. 3D double-reinforced graphene oxide – nanocellulose biomaterial inks for tissue engineered constructs. RSC Adv. 2023;13(34):24053-24063. doi: 10.1039/D3RA02786D
  93. Steward AJ, Kelly DJ. Mechanical regulation of mesenchymal stem cell differentiation. J Anat. 2015;227(6):717-731. doi: 10.1111/joa.12243
  94. Phinney DG. Functional heterogeneity of mesenchymal stem cells: implications for cell therapy. J Cell Biochem. 2012;113(9):2806-2812. doi: 10.1002/jcb.24166
  95. Costa LA, Eiro N, Fraile M, et al. Functional heterogeneity of mesenchymal stem cells from natural niches to culture conditions: implications for further clinical uses. Cell Mol Life Sci. 2021;78(2):447-467. doi: 10.1007/s00018-020-03600-0
  96. Talukdar Y, Rashkow J, Lalwani G, Kanakia S, Sitharaman B. The effects of graphene nanostructures on mesenchymal stem cells. Biomaterials. 2014;35(18):4863-4877. doi: 10.1016/j.biomaterials.2014.02.054
  97. Golub EE, Boesze-Battaglia K. The role of alkaline phosphatase in mineralization. Curr Opin Orthopaed. 2007;18(5):444-448. doi: 10.1097/BCO.0b013e3282630851
  98. Sharma U, Pal D, Prasad R. Alkaline phosphatase: an overview. Indian J Clin Biochem. 2014;29(3):269-278. doi: 10.1007/s12291-013-0408-y
  99. Rutkovskiy A, Stensløkken KO, Vaage IJ. Osteoblast differentiation at a glance. Med Sci Monit Basic Res. 2016;22:95-106. doi: 10.12659/msmbr.901142
  100. Ma H, Feng C, Chang J, Wu C. 3D-printed bioceramic scaffolds: from bone tissue engineering to tumor therapy. Acta Biomaterialia. 2018;79:37-59. doi: 10.1016/j.actbio.2018.08.026
  101. Wu M, Zou L, Jiang L, Zhao Z, Liu J. Osteoinductive and antimicrobial mechanisms of graphene-based materials for enhancing bone tissue engineering. J Tissue Eng Regen Med. 2021;15(11):915-935. doi: 10.1002/term.3239
  102. Shin SR, Li YC, Jang HL, et al. Graphene-based materials for tissue engineering. Adv Drug Deliv Rev. 2016; 105(Pt B):255-274. doi: 10.1016/j.addr.2016.03.007
  103. Farshid B, Lalwani G, Mohammadi MS, et al. Two-dimensional graphene oxide-reinforced porous biodegradable polymeric nanocomposites for bone tissue engineering. J Biomed Mater Res A. 2019;107(6):1143-1153. doi: 10.1002/jbm.a.36606
  104. Catoira MC, Fusaro L, Di Francesco D, Ramella M, Boccafoschi F. Overview of natural hydrogels for regenerative medicine applications. J Mater Sci Mater Med. 2019;30(10):115. doi: 10.1007/s10856-019-6318-7
  105. Zhou L, Tan G, Tan Y, Wang H, Liao J, Ning C. Biomimetic mineralization of anionic gelatin hydrogels: Effect of degree of methacrylation. RSC Adv. 2014;4:21997. doi: 10.1039/c4ra02271h
  106. Castillo Diaz LA, Saiani A, Gough JE, Miller AF. Human osteoblasts within soft peptide hydrogels promote mineralisation in vitro. J Tissue Eng. 2014;5:2041731414539344. doi: 10.1177/2041731414539344
  107. Gerhardt LC, Boccaccini AR. Bioactive glass and glass-ceramic scaffolds for bone tissue engineering. Materials. 2010;3(7):3867-3910. doi: 10.3390/ma3073867
  108. Morgan EF, Unnikrisnan GU, Hussein AI. Bone mechanical properties in healthy and diseased states. Annu Rev Biomed Eng. 2018;20(2018):119-143. doi: 10.1146/annurev-bioeng-062117-121139
  109. Diaz-Rodriguez P, Sánchez M, Landin M. Drug-loaded biomimetic ceramics for tissue engineering. Pharmaceutics. 2018;10(4):272. doi: 10.3390/pharmaceutics10040272
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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
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