journal article·2024-08Open access

Design of magnetic kappa-carrageenan-collagen bioinks for 3D bioprinting

Duarte Almeida, Freya Küppers, Afonso Gusmão, Ana C. Manjua, Catarina F. R. Ferreira, Carla A. M. Portugal, João C. Silva, Paola Sanjuan-Alberte, Frederico Castelo Ferreira

Journal of Materials Science· Volume 59· Issue 31

Abstract

Abstract Bioprinting approaches are of great promise for tissue engineering applications as they allow the fabrication of constructs able to mimic native tissues’ mechanical and topographical features. Additional control over cells fate can be enhanced using stimuli-responsive materials, requiring the development of novel bioinks for this purpose. In this study, bioinks comprising κ-carrageenan, collagen, and magnetic nanoparticles were designed for 3D bioprinting applications. The characterization of this material was performed, where mechanical compressive tests yielded Young’s moduli ranging from 8.25 to 18.4 kPa. Rheological assessments also revealed the shear-thinning behavior of the bioinks and a temperature-dependent gelation. The capability of these bioinks to produce 3D constructs by extrusion bioprinting was established through the printability evaluation and the development of complex structures, supporting the viability and proliferation of mesenchymal stromal cells (MSCs). Finally, as proof-of-concept, it was observed that the secretome of bioprinted MSCs stimulated with an external magnetic field of 80 mT was able to increase the number of tubes formed by human umbilical vein endothelial cells.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: 3D Printing in Biomedical Research · Innovative Microfluidic and Catalytic Techniques Innovation · Cell Image Analysis Techniques

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (73)

Show source-provided references
1. Wang W, Narain R, Zeng H (2020) Hydrogels. Polymer science and nanotechnology. Elsevier, Netherlands, pp 203–24410.1016/B978-0-12-816806-6.00010-8 ↗
2. Zhang G (2012) Biomimicry in biomedical research. Organogenesis 8:101–10210.4161/org.23395 ↗
3. Radulescu D-M, Neacsu IA, Grumezescu A-M, Andronescu E (2022) New Insights of Scaffolds based on hydrogels in tissue engineering. Polymers 14:79910.3390/polym14040799 ↗
4. Huang Y, Zhang X-F, Gao G, Yonezawa T, Cui X (2017) 3D bioprinting and the current applications in tissue engineering. Biotechnol J 12:160073410.1002/biot.201600734 ↗
5. Mandrycky C, Wang Z, Kim K, Kim D-H (2016) 3D bioprinting for engineering complex tissues. Biotechnol Adv 34:422–43410.1016/j.biotechadv.2015.12.011 ↗
6. Marques DMC et al (2022) 3D Bioprinting of novel κ-carrageenan bioinks: an algae-derived polysaccharide. Bioengineering 9:10910.3390/bioengineering9030109 ↗
7. Periyasamy C, Subba Rao PV, Anantharaman P (2019) Harvest optimization to assess sustainable growth and carrageenan yield of cultivated Kappaphycus alvarezii (Doty) Doty in Indian waters. J Appl Phycol 31:587–59710.1007/s10811-018-1562-7 ↗
8. Silva JC et al (2019) Compositional and structural analysis of glycosaminoglycans in cell-derived extracellular matrices. Glycoconj J 36:141–15410.1007/s10719-019-09858-2 ↗
9. Safarpour F et al (2023) Kappa-carrageenan based hybrid hydrogel for soft tissue engineering applications. Biomed Mater. https://doi.org/10.1088/1748-605X/ace0ec10.1088/1748-605X/ace0ec ↗
10. Varghese JS, Chellappa N, Fathima NN (2014) Gelatin–carrageenan hydrogels: role of pore size distribution on drug delivery process. Coll Surf B Biointerfaces 113:346–35110.1016/j.colsurfb.2013.08.049 ↗
11. Croitoru C et al (2020) Physically crosslinked poly (vinyl alcohol)/kappa-carrageenan hydrogels: structure and applications. Polymers 12:56010.3390/polym12030560 ↗
12. Stepanovska J, Supova M, Hanzalek K, Broz A, Matejka R (2021) Collagen bioinks for bioprinting: a systematic review of hydrogel properties, bioprinting parameters, protocols, and bioprinted structure characteristics. Biomedicines 9:113710.3390/biomedicines9091137 ↗
13. Włodarczyk-Biegun MK, Del Campo A (2017) 3D bioprinting of structural proteins. Biomaterials 134:180–20110.1016/j.biomaterials.2017.04.019 ↗
14. Osidak EO, Kozhukhov VI, Osidak MS, Domogatsky SP (2020) Collagen as bioink for bioprinting: a comprehensive review. Int J Bioprint 6(3):17–26. https://doi.org/10.18063/ijb.v6i3.27010.18063/ijb.v6i3.270 ↗
15. El-Husseiny HM et al (2022) Smart/stimuli-responsive hydrogels: cutting-edge platforms for tissue engineering and other biomedical applications. Mater Today Bio 13:10018610.1016/j.mtbio.2021.100186 ↗
16. Almeida D, Sanjuan-Alberte P, Silva JC, Ferreira FC (2023) 3D (bio) printing of magnetic hydrogels: formulation and applications in tissue engineering. Int J Bioprint 10(1):096510.36922/ijb.0965 ↗
17. Zhang J, Huang Q, Du J (2016) Recent advances in magnetic hydrogels: recent advances in magnetic hydrogels. Polym Int 65:1365–137210.1002/pi.5170 ↗
18. Manjua AC, Cabral JMS, Portugal CAM, Ferreira FC (2021) Magnetic stimulation of the angiogenic potential of mesenchymal stromal cells in vascular tissue engineering. Sci Technol Adv Mater 22:461–48010.1080/14686996.2021.1927834 ↗
19. Almeida D. et al. (2024) Design of magnetic κ-carrageenan-collagen bioinks for 3D bioprinting. Preprint at https://doi.org/10.21203/rs.3.rs-4138126/v110.21203/rs.3.rs-4138126/v1 ↗
20. Cruz-Izquierdo Á, Picó EA, López C, Serra JL, Llama MJ (2014) Magnetic cross-linked enzyme aggregates (mCLEAs) of candida antarctica lipase: an efficient and stable biocatalyst for biodiesel synthesis. PLoS ONE 9:e11520210.1371/journal.pone.0115202 ↗
21. Alom N, Peto H, Kirkham GR, Shakesheff KM, White LJ (2018) Bone extracellular matrix hydrogel enhances osteogenic differentiation of C2C12 myoblasts and mouse primary calvarial cells: Bone ECM Hydrogel and Osteogenic Differentiation. J Biomed Mater Res B Appl Biomater 106:900–90810.1002/jbm.b.33894 ↗
22. Gusmão A. et al. (2023) Designing and prototyping a 3D printer for multi-extrusion of thermo—and photocurable hydrogels: enabling affordable and wider access to bioprinting. https://engrxiv.org/preprint/view/2916/version/4158
23. Silva JC et al (2020) Glycosaminoglycan remodeling during chondrogenic differentiation of human bone marrow−/synovial-derived mesenchymal stem/stromal cells under normoxia and hypoxia. Glycoconj J 37:345–36010.1007/s10719-020-09911-5 ↗
24. Carpentier, G. (2012) Angiogenesis Analyzer for ImageJ. http://imagej.nih.gov/ij/macros/toolsets/Angiogenesis%20Analyzer.txt
25. Doane TL, Chuang C-H, Hill RJ, Burda C (2012) Nanoparticle ζ-potentials. Acc Chem Res 45:317–32610.1021/ar200113c ↗
26. Kędzierska M et al (2021) The synthesis methodology of PEGylated Fe3O4@Ag nanoparticles supported by their physicochemical evaluation. Molecules 26:174410.3390/molecules26061744 ↗
27. Darwish MSA, Nguyen NHA, Ševců A, Stibor I (2015) Functionalized magnetic nanoparticles and their effect on escherichia coli and staphylococcus aureus. J Nanomater 2015:1–1010.1155/2015/416012 ↗
28. Cortés-Llanos B et al (2021) Influence of coating and size of magnetic nanoparticles on cellular uptake for in vitro MRI. Nanomaterials 11:288810.3390/nano11112888 ↗
29. Sabuncu AC et al (2012) Probing nanoparticle interactions in cell culture media. Coll Surf B Biointerfaces 95:96–10210.1016/j.colsurfb.2012.02.022 ↗
30. Levy I et al (2015) Bioactive magnetic near Infra-Red fluorescent core-shell iron oxide/human serum albumin nanoparticles for controlled release of growth factors for augmentation of human mesenchymal stem cell growth and differentiation. J Nanobiotechnol 13:3410.1186/s12951-015-0090-8 ↗
31. Ankamwar B (2012) Size and shape effect on biomedical applications of nanomaterials. In: Hudak R (ed) Biomedical engineering—technical applications in medicine https://doi.org/10.5772/4612110.5772/46121 ↗
32. Gavilán H et al (2021) How size, shape and assembly of magnetic nanoparticles give rise to different hyperthermia scenarios. Nanoscale 13:15631–1564610.1039/D1NR03484G ↗
33. Xiao Y, Du J (2020) Superparamagnetic nanoparticles for biomedical applications. J Mater Chem B 8:354–36710.1039/C9TB01955C ↗
34. Chen Y, Hou S (2022) Application of magnetic nanoparticles in cell therapy. Stem Cell Res Ther 13:13510.1186/s13287-022-02808-0 ↗
35. Ganguly S, Margel S (2022) 3D printed magnetic polymer composite hydrogels for hyperthermia and magnetic field driven structural manipulation. Prog Polym Sci 131:10157410.1016/j.progpolymsci.2022.101574 ↗
36. Aliramaji S, Zamanian A, Mozafari M (2017) Super-paramagnetic responsive silk fibroin/chitosan/magnetite scaffolds with tunable pore structures for bone tissue engineering applications. Mater Sci Eng C 70:736–74410.1016/j.msec.2016.09.039 ↗
37. Karahaliloğlu Z, Yalçın E, Demirbilek M, Denkbaş EB (2017) Magnetic silk fibroin e-gel scaffolds for bone tissue engineering applications. J Bioact Compat Polym 32:596–61410.1177/0883911517693635 ↗
38. Feng W et al (2017) A novel composite of collagen-hydroxyapatite/kappa-carrageenan. J Alloys Compd 693:482–48910.1016/j.jallcom.2016.09.234 ↗
39. Lopez-Garcia MDC, Beebe DJ, Crone WC (2010) Young’s modulus of collagen at slow displacement rates. Biomed Mater Eng 20:361–369
40. Rhee S, Puetzer JL, Mason BN, Reinhart-King CA, Bonassar LJ (2016) 3D bioprinting of spatially heterogeneous collagen constructs for cartilage tissue engineering. ACS Biomater Sci Eng 2:1800–180510.1021/acsbiomaterials.6b00288 ↗
41. Gultian KA et al (2022) Human induced mesenchymal stem cells display increased sensitivity to matrix stiffness. Sci Rep 12:848310.1038/s41598-022-12143-2 ↗
42. Czichy C, Spangenberg J, Günther S, Gelinsky M, Odenbach S (2020) Determination of the Young’s modulus for alginate-based hydrogel with magnetite-particles depending on storage conditions and particle concentration. J Magn Magn Mater 501:16639510.1016/j.jmmm.2020.166395 ↗
43. Hu X et al (2019) Adhesive tough magnetic hydrogels with high Fe3O4 content. ACS Appl Mater Interfaces 11:10292–1030010.1021/acsami.8b20937 ↗
44. Ajiteru O et al (2021) A digital light processing 3D printed magnetic bioreactor system using silk magnetic bioink. Biofabrication 13:03410210.1088/1758-5090/abfaee ↗
45. Spangenberg J et al (2021) Bioprinting of magnetically deformable scaffolds. ACS Biomater Sci Eng 7:648–66210.1021/acsbiomaterials.0c01371 ↗
46. Stevens L, Calvert P, Wallace GG, Panhuis MIH (2013) Ionic-covalent entanglement hydrogels from gellan gum, carrageenan and an epoxy-amine. Soft Matter 9:300910.1039/c3sm27413f ↗
47. Tran N-P-D, Yang M-C (2020) The ophthalmic performance of hydrogel contact lenses loaded with silicone nanoparticles. Polymers 12:112810.3390/polym12051128 ↗
48. Lin F et al (2019) Smart cellulose-derived magnetic hydrogel with rapid swelling and deswelling properties for remotely controlled drug release. Cellulose 26:6861–687710.1007/s10570-019-02572-0 ↗
49. Wen C, Lingling L, Li X (2014) Enzymatic and ionic crosslinked gelatin/K‐carrageenan IPN hydrogels as potential biomaterials. J Appl Polym Sci 131(21):app.40975. https://doi.org/10.1002/app.4097510.1002/app.40975 ↗
50. Gao F et al (2019) Magnetic hydrogel with optimally adaptive functions for breast cancer recurrence prevention. Adv Healthc Mater 8:190020310.1002/adhm.201900203 ↗
51. Deng A et al (2021) Preparation of a recombinant collagen-peptide (RHC)-conjugated chitosan thermosensitive hydrogel for wound healing. Mater Sci Eng C 119:11155510.1016/j.msec.2020.111555 ↗
52. Daya R, Xu C, Nguyen N-YT, Liu HH (2022) Angiogenic hyaluronic acid hydrogels with curcumin-coated magnetic nanoparticles for tissue repair. ACS Appl Mater Interfaces 14:11051–1106710.1021/acsami.1c19889 ↗
53. Zhao B et al (2023) Self-healing liquid metal magnetic hydrogels for smart feedback sensors and high-performance electromagnetic shielding. Nano-Micro Lett 15:7910.1007/s40820-023-01043-3 ↗
54. Chung H, Parsons AM, Zheng L (2021) Magnetically controlled soft robotics utilizing elastomers and gels in actuation: a review. Adv Intell Syst 3:200018610.1002/aisy.202000186 ↗
55. Tognato R et al (2019) A stimuli-responsive nanocomposite for 3D anisotropic cell-guidance and magnetic soft robotics. Adv Funct Mater 29:180464710.1002/adfm.201804647 ↗
56. Simińska-Stanny J et al (2022) 4D printing of patterned multimaterial magnetic hydrogel actuators. Addit Manuf 49:102506
57. Lim W et al (2020) Kappa-carrageenan-based dual crosslinkable bioink for extrusion type bioprinting. Polymers 12:237710.3390/polym12102377 ↗
58. Suo H, Zhang J, Xu M, Wang L (2021) Low-temperature 3D printing of collagen and chitosan composite for tissue engineering. Mater Sci Eng C 123:11196310.1016/j.msec.2021.111963 ↗
59. Shi Y et al (2023) Preparation of a 3D printable high-performance GelMA hydrogel loading with magnetic cobalt ferrite nanoparticles. Front Bioeng Biotechnol 11:113219210.3389/fbioe.2023.1132192 ↗
60. Weng L, Chen X, Chen W (2007) Rheological characterization of in situ crosslinkable hydrogels formulated from oxidized dextran and N-carboxyethyl chitosan. Biomacromol 8:1109–111510.1021/bm0610065 ↗
61. De Santis R et al (2016) Viscoelastic properties of rapid prototyped magnetic nanocomposite scaffolds for osteochondral tissue regeneration. Procedia CIRP 49:76–8210.1016/j.procir.2015.07.037 ↗
62. Naghieh S, Chen X (2021) Printability–a key issue in extrusion-based bioprinting. J Pharm Anal 11:564–57910.1016/j.jpha.2021.02.001 ↗
63. Chen Z et al (2019) 3D Printing of Multifunctional Hydrogels. Adv Funct Mater 29:190097110.1002/adfm.201900971 ↗
64. Nasser M, Wu Y, Danaoui Y, Ghosh G (2019) Engineering microenvironments towards harnessing pro-angiogenic potential of mesenchymal stem cells. Mater Sci Eng C 102:75–8410.1016/j.msec.2019.04.030 ↗
65. Loye AM et al (2018) Regulation of mesenchymal stem cell differentiation by nanopatterning of bulk metallic glass. Sci Rep 8:875810.1038/s41598-018-27098-6 ↗
66. Chimene D et al (2020) Nanoengineered osteoinductive bioink for 3D bioprinting bone tissue. ACS Appl Mater Interfaces 12:15976–1598810.1021/acsami.9b19037 ↗
67. Li X, Ma X, Fan D, Zhu C (2012) New suitable for tissue reconstruction injectable chitosan/collagen-based hydrogels. Soft Matter 8:378110.1039/c2sm06994f ↗
68. Silva ED et al (2018) Multifunctional magnetic-responsive hydrogels to engineer tendon-to-bone interface. Nanomed Nanotechnol Biol Med 14:2375–238510.1016/j.nano.2017.06.002 ↗
69. Qian K-Y et al (2020) Injectable ferrimagnetic silk fibroin hydrogel for magnetic hyperthermia ablation of deep tumor. Biomaterials 259:12029910.1016/j.biomaterials.2020.120299 ↗
70. Li F et al (2007) Effects of static magnetic field on human umbilical vessel endothelial cell. J Med Coll PLA 22:106–11010.1016/S1000-1948(07)60023-9 ↗
71. Okano H, Onmori R, Tomita N, Ikada Y (2006) Effects of a moderate-intensity static magnetic field on VEGF-A stimulated endothelial capillary tubule formation in vitro. Bioelectromagnetics 27:628–64010.1002/bem.20246 ↗
72. Paper DH, Vogl H, Franz G, Hoffman R (1995) Defined carrageenan derivatives as angiogenesis inhibitors. Macromol Symp 99:219–22510.1002/masy.19950990123 ↗
73. Rode MP et al (2018) Carrageenan hydrogel as a scaffold for skin-derived multipotent stromal cells delivery. J Biomater Appl 33:422–43410.1177/0885328218795569 ↗