AccScience Publishing / IJB / Volume 10 / Issue 2 / DOI: 10.36922/ijb.2057
Submit to IJB
Cite this article
36
Download
446
Views
Journal Browser
Volume | Year
Issue
Search
Forthcoming Issue
Current Issue
View All
News and Announcements
View All
RESEARCH ARTICLE

Bioprinting with adipose stem cells and hydrogel modified with bioactive glass

Krishna C.R. Kolan1 ,  Apurv Saxena2 ,  Bradley A. Bromet3 ,  Lesa B. Steen4 ,  August T. Bindbeutel1 ,  Julie A. Semon3* ,  Delbert E. Day4 ,  Ming C. Leu1
Show Less
1 Department of Mechanical and Aerospace Engineering, Missouri University of Science and Technology, Rolla, Missouri, United States of America
2 Department of Chemistry, Missouri University of Science and Technology, Rolla, Missouri, United States of America
3 Department of Biological Sciences, Missouri University of Science and Technology, Rolla, Missouri, United States of America
4 Department of Material Science and Engineering, Missouri University of Science and Technology, Rolla, Missouri, United States of America
IJB 2024, 10(2), 2057 https://doi.org/10.36922/ijb.2057
Submitted: 18 October 2023 | Accepted: 31 January 2024 | Published: 1 March 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/ )
Download PDF
Cite
XML
Abstract

Bioprinting research is focused on utilizing growth factors and multiple cell types to create clinically relevant three-dimensional (3D) tissue models using hydrogels. Rheological and biological challenges are two main factors that limit the creation of extrudable bioactive hydrogels. In this study, we investigate incorporation of fast dissolving and bioactive borate glass in different weight to volume percentages (0.075 to 0.6%) to alginate-gelatin (1:1) hydrogel to improve rheological properties and enable bioprinting with bioactive glass. The addition of glass improved the stiffness of the hydrogel. Human adipose-derived mesenchymal stem cells (ASCs) were uniformly mixed in this bioink at 1 × 106 cells/mL concentration, and spheroid specimens were cultured in both static and dynamic culture conditions. Grid-shaped scaffolds measuring ~18 × 18 × 1 mm3 were fabricated with the viable glass concentrations, and ASC viability was evaluated using Live/Dead assay. Despite immediate toxicity, an increased viability after 7 days with 0.15 w/v % or less borate glass content demonstrated the potential in utilizing highly resorbable calcium-releasing biomaterials such as bioactive glasses to modify hydrogels suitable for bioprinting cellularized 3D structures.

Keywords
Bioink
Bioactive glass
Ceramics
Adipose stem cells
Alginate
Gelatin
Funding
This research was funded by the Intelligent Systems Center and the Center for Biomedical Research at the Missouri University of Science and Technology
References
  1. 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
  2. Choudhury D, Anand S, Naing M. The arrival of commercial bioprinters – towards 3D bioprinting revolution! Int J Bioprint. 2018;4(2). doi: 10.18063/IJB.v4i2.139
  3. Gungor-Ozkerim PS, Inci I, Zhang YS, Khademhosseini A, Dokmeci MR. Bioinks for 3D bioprinting: an overview. Biomater Sci. 2018;6(5):915-946. doi: 10.1039/c7bm00765e
  4. Rowley JA, Madlambayan G, Mooney DJ. Alginate hydrogels as synthetic extracellular matrix materials. Biomaterials. 1999;20(1):45-53. doi: 10.1016/S0142-9612(98)00107-0
  5. Smidsrød O, Skjåk-Braek G. Alginate as immobilization matrix for cells. Trends Biotechnol. 1990;8(3):71-78. doi: 10.1016/0167-7799(90)90139-O
  6. Reakasame S, Boccaccini AR. Oxidized alginate-based hydrogels for tissue engineering applications: a review. Biomacromolecules. 2018;19(1):3-21. doi: 10.1021/acs.biomac.7b01331
  7. Jeon O, Alsberg E. Photofunctionalization of alginate hydrogels to promote adhesion and proliferation of human mesenchymal stem cells. Tissue Eng Part A. 2013;19(11- 12):1424-1432. doi: 10.1089/ten.TEA.2012.0581
  8. Alsberg E, Anderson KW, Albeiruti A, Franceschi RT, Mooney DJ. Cell-interactive alginate hydrogels for bone tissue engineering. J Dent Res. 2001;80(11):2025-2029. doi: 10.1177/00220345010800111501
  9. Rastogi P, Kandasubramanian B. Review of alginate-based hydrogel bioprinting for application in tissue engineering. Biofabrication. 2019;11(4):042001. doi: 10.1088/1758-5090/ab331e
  10. Giuseppe M Di, Law N, Webb B, et al. Mechanical behaviour of alginate-gelatin hydrogels for 3D bioprinting. J Mech Behav Biomed Mater. 2018;79:150-157. doi: 10.1016/J.JMBBM.2017.12.018
  11. Chung JHY, Naficy S, Yue Z, et al. Bio-ink properties and printability for extrusion printing living cells. Biomater Sci. 2013;1(7):763. doi: 10.1039/c3bm00012e
  12. Jiang T, Munguia-Lopez J, Flores-Torres S, et al. Bioprintable alginate/gelatin hydrogel 3D in vitro model systems induce cell spheroid formation. J Vis Exp. 2018;(137):e57826. doi: 10.3791/57826
  13. Li Z, Huang S, Liu Y, et al. Tuning alginate-gelatin bioink properties by varying solvent and their impact on stem cell behavior. Sci Rep. 2018;8(1):8020. doi: 10.1038/s41598-018-26407-3
  14. Duan B, Hockaday LA, Kang KH, Butcher JT. 3D Bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res Part A. 2013;101A(5): 1255-1264. doi: 10.1002/jbm.a.34420
  15. Rahaman MN, Day DE, Sonny Bal B, et al. Bioactive glass in tissue engineering. Acta Biomater. 2011;7(6):2355-2373. doi: 10.1016/j.actbio.2011.03.016
  16. Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials. 2006;27(15): 2907-2915. doi: 10.1016/j.biomaterials.2006.01.017
  17. Miguez-Pacheco V, Hench LL, Boccaccini AR. Bioactive glasses beyond bone and teeth: emerging applications in contact with soft tissues. Acta Biomater. 2015;13:1-15. doi: 10.1016/J.ACTBIO.2014.11.004
  18. Richard M. Bioactive Behavior of a Borate Glass. Master’s Theses. Missouri University of Science and Technology; 2000. 
  19. Jung S. Borate Based Bioactive Glass Scaffolds for Hard and Soft Tissue Engineering. Dissertation. Missouri University of Science and Technology; 2010.
  20. George J. Dissolution of Borate Glasses and Precipitation of Phosphate Compounds. Dissertation. Missouri University of Science and Technology; 2015.
  21. Nychka JA, Mazur SLR, Kashyap S, Li D, Yang F. Dissolution of bioactive glasses: the effects of crystallinity coupled with stress. JOM. 2009;61(9):45-51. doi: 10.1007/s11837-009-0132-5
  22. Liu X, Rahaman MN, Day DE. Conversion of melt-derived microfibrous borate (13-93B3) and silicate (45S5) bioactive glass in a simulated body fluid. J Mater Sci Mater Med. 2013;24(3):583-595. doi: 10.1007/s10856-012-4831-z
  23. Zhao F, Yang Z, Xiong H, Yan Y, Chen X, Shao L. A bioactive glass functional hydrogel enhances bone augmentation via synergistic angiogenesis, self-swelling and osteogenesis. Bioact Mater. 2023;22:201-210. doi: 10.1016/j.bioactmat.2022.09.007
  24. Zhu H, Monavari M, Zheng K, et al. 3D bioprinting of multifunctional dynamic nanocomposite bioinks incorporating Cu-doped mesoporous bioactive glass nanoparticles for bone tissue engineering. Small. 2022;18(12):2104996. doi: 10.1002/smll.202104996
  25. Monavari M, Homaeigohar S, Medhekar R, et al. A 3D-printed wound-healing material composed of alginate dialdehyde-gelatin incorporating astaxanthin and borate bioactive glass microparticles. ACS Appl Mater Interfaces. 2023;15(44):50626-50637. doi: 10.1021/acsami.2c23252
  26. Kolan KCR, Semon JA, Bromet B, Day DE, Leu MC. Bioprinting with human stem cells-laden alginate-gelatin bioink and bioactive glass for tissue engineering. Int J Bioprint. 2019;5(2.2):3. doi: 10.18063/ijb.v5i2.2.204
  27. Jung SB. Borate based bioactive glass scaffolds for hard and soft tissue engineering. Zhurnal Eksp i Teor Fiz. 2010;389.
  28. Watters R, Brown R, Day D. Angiogenic effect of bioactive borate glass microfibers and beads in the hairless mouse. Bioact Glas. 2015;1(1). doi: 10.1515/bglass-2015-0017
  29. Lin Y, Brown RF, Jung SB, Day DE. Angiogenic effects of borate glass microfibers in a rodent model. J Biomed Mater Res Part A. 2014;102(12):4491-4499. doi: 10.1002/jbm.a.35120
  30. Thyparambil N, Gutgesell L, Bromet B, et al. Bioactive borate glass triggers phenotypic changes in adipose stem cells. J Mater Sci Mater Med. 2020;31(4):35. doi: 10.1007/s10856-020-06366-w
  31. Dykstra JA, Facile T, Patrick RJ, et al. Concise review: fat and furious: harnessing the full potential of adipose-derived stromal vascular fraction. Stem Cells Transl Med. 2017;6(4):1096-1108. doi: 10.1002/sctm.16-0337
  32. Gimble JM, Guilak F, Bunnell BA. Clinical and preclinical translation of cell-based therapies using adipose tissue-derived cells. Stem Cell Res Ther. 2010;1(2):19. doi: 10.1186/scrt19
  33. Bourin P, Bunnell BA, Casteilla L, et al. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy. 2013;15(6):641-648. doi: 10.1016/j.jcyt.2013.02.006
  34. Kolan KCR, Semon JA, Bindbeutel AT, Day DE, Leu MC. Bioprinting with bioactive glass loaded polylactic acid composite and human adipose stem cells. Bioprinting. 2020;18:e00075. doi: 10.1016/j.bprint.2020.e00075
  35. Thyparambil NJ, Gutgesell LC, Hurley CC, Flowers LE, Day DE, Semon JA. Adult stem cell response to doped bioactive borate glass. J Mater Sci Mater Med. 2020;31(2):1-8. doi: 10.1007/s10856-019-6353-4 
  36. Suvarnapathaki S, Nguyen MA, Wu X, Nukavarapu SP, Camci-Unal G. Synthesis and characterization of photocrosslinkable hydrogels from bovine skin gelatin. RSC Adv. 2019;9:13016-13025. doi: 10.1039/c9ra00655a
  37. Okay O. General Properties of Hydrogels. Berlin, Heidelberg: Springer; 2009:1-14. doi: 10.1007/978-3-540-75645-3_1
  38. Jung S, Day D. Conversion kinetics of silicate, borosilicate, and borate bioactive glasses to hydroxyapatite. Phys Chem Glas. 2009;50(2):85-88.
  39. Liu X, Pan H, Fu H, Fu Q, Rahaman MN, Huang W. Conversion of borate-based glass scaffold to hydroxyapatite in a dilute phosphate solution. Biomed Mater. 2010;5(1):015005. doi: 10.1088/1748-6041/5/1/015005
  40. George JL, Brow RK. In-situ characterization of borate glass dissolution kinetics by μ-Raman spectroscopy. J Non Cryst Solids. 2015;426:116-124. doi: 10.1016/J.JNONCRYSOL.2015.07.003
  41. Fu Q, Rahaman MN, Fu H, Liu X. Silicate, borosilicate, and borate bioactive glass scaffolds with controllable degradation rate for bone tissue engineering applications. I. Preparation and in vitro degradation. J Biomed Mater Res Part A. 2010;95A(1):164-171. doi: 10.1002/jbm.a.32824
  42. Huebsch N, Arany PR, Mao AS, et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater. 2010;9(6):518-526. doi: 10.1038/nmat2732
  43. Chaudhuri O, Gu L, Klumpers D, et al. Hydrogels with tunable stress relaxation regulate stem cell fate and activity. Nat Mater. 2016;15(3):326-334. doi: 10.1038/nmat4489
  44. Qazi TH, Hafeez S, Schmidt J, Duda GN, Boccaccini AR, Lippens E. Comparison of the effects of 45S5 and 1393 bioactive glass microparticles on hMSC behavior. J Biomed Mater Res A. 2017;105(10):2772-2782. doi: 10.1002/jbm.a.36131
  45. Hoppe A, Boccaccini AR. Biological impact of bioactive glasses and their dissolution products. Front Oral Biol. 2015;17:22-32. doi: 10.1159/000381690
  46. Wang X, Tolba E, Schröder HC, et al. Effect of bioglass on growth and biomineralization of SaOS-2 cells in hydrogel after 3D cell bioprinting. PLoS One. 2014;9(11):e112497. doi: 10.1371/journal.pone.0112497
  47. Sarker B, Singh R, Silva R, et al. Evaluation of fibroblasts adhesion and proliferation on alginate-gelatin crosslinked hydrogel. PLoS One. 2014;9(9):e107952. doi: 10.1371/journal.pone.0107952
  48. Couto DS, Hong Z, Mano JF. Development of bioactive and biodegradable chitosan-based injectable systems containing bioactive glass nanoparticles. Acta Biomater. 2009;5(1): 115-123. doi: 10.1016/j.actbio.2008.08.006
  49. Nikpour P, Salimi-Kenari H, Fahimipour F, et al. Dextran hydrogels incorporated with bioactive glass-ceramic: nanocomposite scaffolds for bone tissue engineering. Carbohydr Polym. 2018;190:281-294. doi: 10.1016/j.carbpol.2018.02.083
  50. Killion JA, Kehoe S, Geever LM, et al. Hydrogel/bioactive glass composites for bone regeneration applications: synthesis and characterisation. Mater Sci Eng C. 2013;33(7):4203-4212. doi: 10.1016/j.msec.2013.06.013
  51. Moreira CDF, Carvalho SM, Sousa RG, Mansur HS, Pereira MM. Nanostructured chitosan/gelatin/bioactive glass in situ forming hydrogel composites as a potential injectable matrix for bone tissue engineering. Mater Chem Phys. 2018;218:304-316. doi: 10.1016/j.matchemphys.2018.07.039
  52. Gantar A, Drnovšek N, Casuso P, et al. Injectable and self-healing dynamic hydrogel containing bioactive glass nanoparticles as a potential biomaterial for bone regeneration. RSC Adv. 2016;6(73):69156-69166. doi: 10.1039/C6RA17327F 
  53. Zhu N, Chatzistavrou X, Papagerakis P, Ge L, Qin M, Wang Y. Silver-doped bioactive glass/chitosan hydrogel with potential application in dental pulp repair. ACS Biomater Sci Eng. 2019;5(9):4624-4633. doi: 10.1021/acsbiomaterials.9b00811
  54. Washio A, Teshima H, Yokota K, Kitamura C, Tabata Y. Preparation of gelatin hydrogel sponges incorporating bioactive glasses capable for the controlled release of fibroblast growth factor-2. J Biomater Sci Polym Ed. 2019;30(1):49-63. doi: 10.1080/09205063.2018.1544474
  55. Leite ÁJ, Sarker B, Zehnder T, Silva R, Mano JF, Boccaccini AR. Bioplotting of a bioactive alginate dialdehyde-gelatin composite hydrogel containing bioactive glass nanoparticles. Biofabrication. 2016;8(3):035005. doi: 10.1088/1758-5090/8/3/035005
  56. Douglas TEL, Dziadek M, Gorodzha S, et al. Novel injectable gellan gum hydrogel composites incorporating Zn- and Sr-enriched bioactive glass microparticles: High-resolution X-ray microcomputed tomography, antibacterial and in vitro testing. J Tissue Eng Regen Med. 2018;12(6): 1313-1326. doi: 10.1002/term.2654
  57. Sevari SP, Shahnazi F, Chen C, Mitchell JC, Ansari S, Moshaverinia A. Bioactive glass‐containing hydrogel delivery system for osteogenic differentiation of human dental pulp stem cells. J Biomed Mater Res Part A. 2020;108(3):557-564. doi: 10.1002/jbm.a.36836
  58. Vuornos K, Ojansivu M, Koivisto JT, et al. Bioactive glass ions induce efficient osteogenic differentiation of human adipose stem cells encapsulated in gellan gum and collagen type I hydrogels. Mater Sci Eng C. 2019;99:905-918. doi: 10.1016/j.msec.2019.02.035
  59. Sun W, Starly B, Daly AC, et al. The bioprinting roadmap. Biofabrication. 2020;12(2):022002. doi: 10.1088/1758-5090/ab5158
Conflict of interest
The authors declare no conflicts of interest.
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