AccScience Publishing / IJB / Online First / DOI: 10.36922/ijb.1830
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RESEARCH ARTICLE

Light-based and cost-effective bioprinting of musculoskeletal GelMA constructs enriched with mesoporous bioactive glass nanoparticles

Víctor Hugo Sánchez-Rodríguez1 ,  Juan Enrique Pérez-Cortez2 ,  Salvador Gallegos-Martínez1 ,  Cristina Chuck-Hernández2,3 ,  Ciro A. Rodriguez2,4 ,  Aldo R. Boccaccini5 ,  Elisa Vázquez-Lepe2,4 ,  Mario Moisés Alvarez1 ,  Grissel Trujillo-de Santiago1* ,  José Israel Martínez-López2,4,6*
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1 Centro de Biotecnología-FEMSA, Tecnologico de Monterrey, Monterrey, Nuevo León, Mexico
2 Escuela de Ingeniería y Ciencias, Tecnologico de Monterrey, Monterrey, Nuevo León, Mexico
3 Institute for Obesity Research, Tecnologico de Monterrey, Monterrey, Nuevo León, Mexico
4 Laboratorio Nacional de Manufactura Aditiva MADiT, Apodaca, Nuevo León, Mexico
5 Institute of Biomaterials, University of Erlangen-Nuremberg, Erlangen, Germany
6 Centro de Investigación Numericalc, Monterrey, Nuevo León, Mexico
IJB 2024, 10(4), 1830 https://doi.org/10.36922/ijb.1830
Submitted: 14 September 2023 | Accepted: 20 May 2024 | Published: 5 August 2024
© 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

Bioprinting represents a promising technique for fabricating three-dimensional (3D) constructs with high-resolution and controlled architecture. However, many bioprinting technologies rely on expensive extrusion systems, which may compromise cell viability due to harsh processing conditions. This study presents the fabrication and characterization of musculoskeletal tissue in gelatin methacryloyl [GelMA]-based nanocomposite 3D constructs (comprising GelMA and mesoporous bioactive glass nanoparticles [MBGNs]) using a cost-effective, light-based bioprinting (LBB) system. We demonstrated that our strategy can produce high-resolution constructs (approximately 250 μm) while maintaining high cell viabilities (above 85%) for extended periods (weeks of culture). Furthermore, the nanocomposite constructs could facilitate the maturation of musculoskeletal tissue derived from C2C12 cells, as indicated by assessments of cell viability, elongation, and alignment over time. Our results suggested that the bioprinting approach outlined in this study allows for precise control of architecture, while creating a conducive environment for cell growth and tissue formation. These findings also highlighted the potential of the proposed LBB system to advance musculoskeletal tissue engineering for regenerative medicine applications.

Keywords
Light-based bioprinting
Mesoporous bioactive glass nanoparticles
Bioactive glass
Musculoskeletal tissue
GelMA
Bioprinting
Funding
Víctor Sánchez, Juan Enrique Pérez, and Salvador Gallegos acknowledge the grant support of the Mexican National Council for Humanities, Science, and Technology (CONAHCYT).
Conflict of interest
The authors declare no conflicts of interest.
References
  1. Downing K, Prisby R, Varanasi V, Zhou J, Pan Z, Brotto M. Old and new biomarkers for volumetric muscle loss. Curr Opin Pharmacol. 2021;59:61-69. doi: 10.1016/j.coph.2021.05.001
  2. McFaline-Figueroa J, Schifino AG, Nichenko AS, et al. Pharmaceutical agents for contractile-metabolic dysfunction after volumetric muscle loss. Tissue Eng Part A. 2022; 28(17-18):795-806. doi: 10.1089/ten.TEA.2022.0036
  3. Ahuja N, Awad K, Peper S, Brotto M, Varanasi V. Mini review: biomaterials in repair and regeneration of nerve in a volumetric muscle loss. Neurosci Lett. 2021;762: 136145. doi: 10.1016/j.neulet.2021.136145
  4. Tavares-Negrete JA, Pedroza-González SC, Frías-Sánchez AI, et al. Supplementation of GelMA with minimally processed tissue promotes the formation of densely packed skeletal-muscle-like tissues. ACS Biomater Sci Eng. 2023;9(6):3462-3475. doi: 10.1021/acsbiomaterials.2c01521
  5. Carnes ME, Pins GD. Skeletal muscle tissue engineering: biomaterials-based strategies for the treatment of volumetric muscle loss. Bioengineering (Basel). 2020;7(3):85. doi: 10.3390/bioengineering7030085
  6. Frías-Sánchez AI, Quevedo-Moreno DA, Samandari M, et al. Biofabrication of muscle fibers enhanced with plant viral nanoparticles using surface chaotic flows. Biofabrication. 2021;13(3). doi: 10.1088/1758-5090/abd9d7
  7. Bolívar-Monsalve EJ, Ceballos-González CF, Borrayo- Montaño KI, et al. Continuous chaotic bioprinting of skeletal muscle-like constructs. Bioprinting. 2021; 21:e00125. doi: 10.1016/j.bprint.2020.e00125
  8. Bolívar-Monsalve EJ, Ceballos-González CF, Chávez- Madero C, et al. One-step bioprinting of multi-channel hydrogel filaments using chaotic advection: fabrication of pre-vascularized muscle-like tissues. Adv Healthc Mater. 2022;11(24):e2200448. doi: 10.1002/adhm.202200448
  9. Zhuang P, An J, Chua CK, Tan LP. Bioprinting of 3D in vitro skeletal muscle models: a review. Maters Design. 2020;193:108794. doi: 10.1016/j.matdes.2020.108794
  10. Daly AC, Prendergast ME, Hughes AJ, Burdick JA. Bioprinting for the biologist. Cell. 2021;184(1):18-32. doi: 10.1016/j.cell.2020.12.002
  11. Samandari M, Quint J, Rodríguez-de la Rosa A, Sinha I, Pourquié O, Tamayol A. Bioinks and bioprinting strategies for skeletal muscle tissue engineering. Adv Mater. 2022;34(12):2105883. doi: 10.1002/adma.202105883
  12. Nieto D, Marchal Corrales JA, Jorge de Mora A, Moroni L. Fundamentals of light-cell–polymer interactions in photo-cross-linking based bioprinting. APL Bioeng. 2020;4(4):041502. doi: 10.1063/5.0022693
  13. Ege D, Hasirci V. Is 3D printing promising for osteochondral tissue regeneration? ACS Appl Bio Mater. 2023;6(4): 1431-1444. doi: 10.1021/acsabm.3c00093
  14. Arcaute K, Mann B, Wicker R. Stereolithography of spatially controlled multi-material bioactive poly(ethylene glycol) scaffolds. Acta Biomater. 2010;6(3):1047-1054. doi: 10.1016/j.actbio.2009.08.017
  15. 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
  16. Levato R, Dudaryeva O, Garciamendez-Mijares CE, et al. Light-based vat-polymerization bioprinting. Nature Reviews Methods Primers. 2023;3(1):47. doi: 10.1038/s43586-023-00231-0
  17. Ying G, Jiang N, Yu C, Zhang YS. Three-dimensional bioprinting of gelatin methacryloyl (GelMA). Bio-des Manuf. 2018;1(4):215-224. doi: 10.1007/s42242-018-0028-8
  18. Mamidi N, Velasco Delgadillo RM, Barrera EV. Covalently functionalized carbon nano-onions integrated gelatin methacryloyl nanocomposite hydrogel containing γ-cyclodextrin as drug carrier for high-performance ph-triggered drug release. Pharmaceuticals (Basel).2021;14(4):291. doi: 10.3390/ph14040291
  19. Mamidi N, Villela Castrejón J, González-Ortiz A. Rational design and engineering of carbon nano-onions reinforced natural protein nanocomposite hydrogels for biomedical applications. J Mech Behav Biomed Mater. 2020;104: 103696. doi: 10.1016/j.jmbbm.2020.103696
  20. Daly AC, Critchley SE, Rencsok EM, Kelly DJ. A comparison of different bioinks for 3D bioprinting of fibrocartilage and hyaline cartilage. Biofabrication. 2016;8(4):045002. doi: 10.1088/1758-5090/8/4/045002
  21. Pedroza-González SC, Rodriguez-Salvador M, Pérez- Benítez BE, Alvarez MM, Trujillo-de Santiago G. Bioinks for 3D bioprinting: a scientometric analysis of two decades of progress. Int J Bioprint. 2021;7(2):333. doi: 10.18063/ijb.v7i2.337
  22. 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
  23. Jones JR. Review of bioactive glass: from Hench to hybrids. Acta Biomater. 2013;9(1):4457-4486. doi: 10.1016/j.actbio.2012.08.023
  24. El-Fiqi A, Kim TH, Kim M, et al. Capacity of mesoporous bioactive glass nanoparticles to deliver therapeutic molecules. Nanoscale. 2012;4(23):7475-7488. doi: 10.1039/C2NR31775C
  25. El-Rashidy A, Roether J, Harhaus L, Kneser U, Boccaccini AR. Regenerating bone with bioactive glass scaffolds: a review of in vivo studies in bone defect models. Acta Biomater. 2017;62:1-28. doi: 10.1016/j.actbio.2017.08.030
  26. Hasan A, Morshed M, Memic A, Hassan S, Webster TJ, Marei HES. Nanoparticles in tissue engineering: applications, challenges and prospects. Int J Nanomedicine. 2018;13: 5637-5655. doi: 10.2147/IJN.S153758
  27. Chen QZ, Thompson ID, Boccaccini AR. 45S5 Bioglass®- derived glass–ceramic scaffolds for bone tissue engineering. Biomaterials. 2006;27(11):2414-2425. doi: 10.1016/j.biomaterials.2005.11.025
  28. Jia W, Hu H, Li A, et al. Glass-activated regeneration of volumetric muscle loss. Acta Biomater. 2020;103:306-317. doi: 10.1016/j.actbio.2019.12.007
  29. Ege D, Nawaz Q, Beltrán AM, Boccaccini AR. Effect of boron-doped mesoporous bioactive glass nanoparticles on c2c12 cell viability and differentiation: potential for muscle tissue application. ACS Biomater Sci Eng. 2022;8(12): 5273-5283. doi: 10.1021/acsbiomaterials.2c00876
  30. Winston DD, Li T, Lei B. Bioactive nanoglass regulating the myogenic differentiation and skeletal muscle regeneration. Regenerative Biomater. 2023;10:rbad059. doi: 10.1093/rb/rbad059
  31. Rahaman MN, Day DE, Bal BS, et al. Bioactive glass in tissue engineering. Acta Biomater. 2011;7(6):2355-2373. doi: 10.1016/j.actbio.2011.03.016
  32. Ceballos-González CF, Bolívar Monsalve EJ, Quevedo‐ Moreno DA, et al. Plug‐and‐play multimaterial chaotic printing/bioprinting to produce radial and axial micropatterns in hydrogel filaments. Adv Mater Technol. 2023;8(17):202202208. doi: 10.1002/admt.202202208
  33. Yang X, Dargaville BL, Hutmacher DW. Elucidating the molecular mechanisms for the interaction of water with polyethylene glycol-based hydrogels: influence of ionic strength and gel network structure. Polymers (Basel). 2021;13(6):845. doi: 10.3390/polym13060845
  34. Vigata M, Meinert C, Bock N, Dargaville BL, Hutmacher DW. Deciphering the molecular mechanism of water interaction with gelatin methacryloyl hydrogels: role of ionic strength, ph, drug loading and hydrogel network characteristics. Biomedicines. 2021;9(5):574. doi: 10.3390/biomedicines9050574
  35. Pérez Cortez JE, Sánchez-Rodríguez VH, Vázquez E, Trujillo-de Santiago G, Alvarez MM, Martínez-López JI. Retrofitting of an affordable 3D printer: towards a material efficient and low-cost bioprinting system. Procedia CIRP. 2022;110:150-155. doi: 10.1016/j.procir.2022.06.028
  36. 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
  37. Font Tellado S, Balmayor ER, Van Griensven M. Strategies to engineer tendon/ligament-to-bone interface: biomaterials, cells and growth factors. Adv Drug Deliv Rev. 2015; 94:126-140. doi: 10.1016/j.addr.2015.03.004
  38. Gao L, Zhou Y, Peng J, et al. A novel dual-adhesive and bioactive hydrogel activated by bioglass for wound healing. NPG Asia Mater. 2019;11(1):66. doi: 10.1038/s41427-019-0168-0
  39. Zöllner AM, Abilez OJ, Böl M, Kuhl E. Stretching skeletal muscle: chronic muscle lengthening through sarcomerogenesis. PLoS One. 2012;7(10): e45661. doi: 10.1371/journal.pone.0045661
  40. Vasita R. A review on extracellular matrix mimicking strategies for an artificial stem cell niche. Polym Rev. 2015;55(4):561-595. doi: 10.1080/15583724.2015.1040552
  41. Yin H, Price F, Rudnicki MA. Satellite cells and the muscle stem cell niche. Physiol Rev. 2013;93(1):23-67. doi: 10.1152/physrev.00043.2011
  42. Relaix F, Zammit PS. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development. 2012;139(16):2845-2856. doi: 10.1242/dev.069088
  43. Heinemeier KM, Schjerling P, Heinemeier J, Magnusson SP, Kjaer M. Lack of tissue renewal in human adult Achilles tendon is revealed by nuclear bomb 14C. FASEB J. 2013;27(5):2074-2079. doi: 10.1096/fj.12-225599
  44. Ogneva IV, Lebedev DV, Shenkman BS. Transversal stiffness and Young’s modulus of single fibers from rat soleus muscle probed by atomic force microscopy. Biophys J. 2010;98(3):418-424. doi: 10.1016/j.bpj.2009.10.028
  45. Collinsworth AM, Zhang S, Kraus WE, Truskey GA. Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Physiol Cell Physiol. 2002;283(4):C1219-C1227. doi: 10.1152/ajpcell.00502.2001
  46. Elvitigala KCML, Mubarok W, Sakai S. Tuning the crosslinking and degradation of hyaluronic acid/gelatin hydrogels using hydrogen peroxide for muscle cell sheet fabrication. Soft Matter. 2023;19(31):5880-5887. doi: 10.1039/D3SM00560G
  47. Gao H, Xiao J, Wei Y, Wang H, Wan H, Liu S. Regulation of myogenic differentiation by topologically microgrooved surfaces for skeletal muscle tissue engineering. ACS Omega. 2021;6(32):20931-20940. doi: 10.1021/acsomega.1c02347
  48. Wu C, Chin CSM, Huang Q, et al. Rapid nanomolding of nanotopography on flexible substrates to control muscle cell growth with enhanced maturation. Microsyst Nanoeng. 2021;7(1):1-15. doi: 10.1038/s41378-021-00316-4
  49. Yu K, Zhang X, Sun Y, et al. Printability during projection-based 3D bioprinting. Bioact Mater. 2022;11:254-267. doi: 10.1016/j.bioactmat.2021.09.021

 

 



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International Journal of Bioprinting, Electronic ISSN: 2424-8002 Print ISSN: 2424-7723, Published by AccScience Publishing
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