Cross-Linked Gelatine by Modified Dextran as a Potential Bioink Prepared by a Simple and Non-Toxic Process
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
DKRVO 494 (RP/CPS/2020/003)
Ministry of Education, Youth and Sports of the Czech republic
Reg. No. CZ.02.2.69/0.0/0.0/19_073/0016941
Junior Grants of TBU in Zlín,
CZ.1.05/2.1.00/19.0376
CEBIA-Tech Instrumentation
20-498 28732S
Czech Science Foundation
PubMed
35160381
PubMed Central
PMC8838658
DOI
10.3390/polym14030391
PII: polym14030391
Knihovny.cz E-zdroje
- Klíčová slova
- 3D printing, microextrusion, cell distribution, gelatine-dextran, hydrogel, rheology,
- Publikační typ
- časopisecké články MeSH
Essential features of well-designed materials intended for 3D bioprinting via microextrusion are the appropriate rheological behavior and cell-friendly environment. Despite the rapid development, few materials are utilizable as bioinks. The aim of our work was to design a novel cytocompatible material facilitating extrusion-based 3D printing while maintaining a relatively simple and straightforward preparation process without the need for harsh chemicals or radiation. Specifically, hydrogels were prepared from gelatines coming from three sources-bovine, rabbit, and chicken-cross-linked by dextran polyaldehyde. The influence of dextran concentration on the properties of hydrogels was studied. Rheological measurements not only confirmed the strong shear-thinning behavior of prepared inks but were also used for capturing cross-linking reaction kinetics and demonstrated quick achievement of gelation point (in most cases < 3 min). Their viscoelastic properties allowed satisfactory extrusion, forming a self-supported multi-layered uniformly porous structure. All gelatin-based hydrogels were non-cytototoxic. Homogeneous cells distribution within the printed scaffold was confirmed by fluorescence confocal microscopy. In addition, no disruption of cells structure was observed. The results demonstrate the great potential of the presented hydrogels for applications related to 3D bioprinting.
Zobrazit více v PubMed
Wei L., Jovina T., Wai Y., May W. Proof-of-concept: 3D bioprinting of pigmented human skin constructs. Biofabrication. 2018;10:1758–5090. doi: 10.1088/1758-5090/aa9e1e. PubMed DOI
Billiet T., Vandenhaute M., Schelfhout J., Vlierberghe S.V., Dubruel P. A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials. 2012;33:6020–6041. doi: 10.1016/j.biomaterials.2012.04.050. PubMed DOI
Gopinathan J., Noh I. Recent trends in bioinks for 3D printing. Biomater. Res. 2018;22:11. doi: 10.1186/s40824-018-0122-1. PubMed DOI PMC
Ashammakhi N., Ahadian S., Xu C., Montazerian H., Ko H., Nasiri R., Barros N., Khademhosseini A. Bioinks and bioprinting technologies to make heterogeneous and biomimetic tissue constructs. Mater. Today Bio. 2019;1:100008. doi: 10.1016/j.mtbio.2019.100008. PubMed DOI PMC
Gungor-Ozkerim P., Inci I., Zhang Y., Khademhosseini S., Dokmeci M. Bioinks for 3D bioprinting: An overview. Biomater. Sci. 2018;6:915–946. doi: 10.1039/C7BM00765E. PubMed DOI PMC
Dorishetty P., Dutta N., Choudhury N. Bioprintable tough hydrogels for tissue engineering applications. Adv. Colloid Interface Sci. 2020;281:102163. doi: 10.1016/j.cis.2020.102163. PubMed DOI
Chimene D., Kaunas R., Gaharwar A. Hydrogel Bioink Reinforcement for Additive Manufacturing: A Focused Review of Emerging Strategies. Adv. Mater. 2020;32:1902026–1902048. doi: 10.1002/adma.201902026. PubMed DOI
Chung S.H., Son S., Min J. The nanostructure effect on the adhesion and growth rates of epithelial cells with well-defined nanoporous alumina substrates. Nanotechnology. 2010;21:125104. doi: 10.1088/0957-4484/21/12/125104. PubMed DOI
Ermis M., Antmen E., Hasirci V. Micro and Nanofabrication methods to control cell-substrate interactions and cell behavior: A review from the tissue engineering perspective. Bioact. Mater. 2018;3:355–369. doi: 10.1016/j.bioactmat.2018.05.005. PubMed DOI PMC
Buskermolen A., Suresh H., Shishvan S., Vigliotti A., DeSimone A., Kurniawan N., Bouten C., Deshpande V. Entropic Forces Drive Cellular Contact Guidance. Biophys. J. 2019;116:1994–2008. doi: 10.1016/j.bpj.2019.04.003. PubMed DOI PMC
Smith C., Stone A., Parkhill R., Stewart R., Simpkins M., Kachurin A., Warren W., Williams S. Three-Dimensional BioAssembly Tool for Generating Viable Tissue-Engineered Constructs. Tissue Eng. 2004;10:1566–1576. doi: 10.1089/ten.2004.10.1566. PubMed DOI
Blaeser A., Campos D.D., Puster U., Richtering W., Stevens M., Fischer H. Controlling Shear Stress in 3D Bioprinting is a Key Factor to Balance Printing Resolution and Stem Cell Integrity. Adv. Healthc. Mater. 2016;5:326–333. doi: 10.1002/adhm.201500677. PubMed DOI
Hölzl K., Lin S., Tytgat L., Vlierberghe S.V., Gu L., Ovsianikov A. Bioink properties before, during and after 3D bioprinting. Biofabrication. 2016;8:032002–032020. doi: 10.1088/1758-5090/8/3/032002. PubMed DOI
Mackay M. The importance of rheological behavior in the additive manufacturing technique material extrusion. J. Rheol. 2018;62:1549–1561. doi: 10.1122/1.5037687. DOI
Mori A.D., Fernández M.P., Blunn G., Tozzi G., Roldo M. 3D Printing and Electrospinning of Composite Hydrogels for Cartilage and Bone Tissue Engineering. Polymers. 2018;10:285. doi: 10.3390/polym10030285. PubMed DOI PMC
Mazzocchi A., Devarasetty M., Huntwork R., Soker S., Skardal A. Optimization of collagen type I-hyaluronan hybrid bioink for 3D bioprinted liver microenvironments. Biofabrication. 2019;11:015003–015014. doi: 10.1088/1758-5090/aae543. PubMed DOI PMC
Caló E., Khutoryanskiy V. Biomedical applications of hydrogels: A review of patents and commercial products. Eur. Polym. J. 2015;65:252–267. doi: 10.1016/j.eurpolymj.2014.11.024. DOI
Gřundělová L., Gregorova A., Mráček A., Vícha R., Smolka P., Minařík A. Viscoelastic and mechanical properties of hyaluronan films and hydrogels modified by carbodiimide. Carbohydr. Polym. 2015;119:142–148. doi: 10.1016/j.carbpol.2014.11.049. PubMed DOI
Dababneh A., Ozbolat I. Bioprinting Technology: A Current State-of-the-Art Review. J. Manuf. Sci. Eng. 2014;136:061016. doi: 10.1115/1.4028512. DOI
Jungst T., Smolan W., Schacht K., Scheibel T., Groll J. Strategies and Molecular Design Criteria for 3D Printable Hydrogels. Chem. Rev. 2016;116:1496–1539. doi: 10.1021/acs.chemrev.5b00303. PubMed DOI
Khunmanee S., Jeong Y., Park H. Crosslinking method of hyaluronic-based hydrogel for biomedical applications. J. Tissue Eng. 2017;8:2041731417726464–2041731417726479. doi: 10.1177/2041731417726464. PubMed DOI PMC
Musilová L., Mráček A., Kovalcik A., Smolka P., Minařík A., Humpolíček P., Vícha R., Ponížil P. Hyaluronan hydrogels modified by glycinated Kraft lignin: Morphology, swelling, viscoelastic properties and biocompatibility. Carbohydr. Polym. 2018;181:394–403. doi: 10.1016/j.carbpol.2017.10.048. PubMed DOI
Poldervaart M., Goversen B., de Ruijter M., Abbadessa A., Melchels F., Öner F., Dhert W., Vermonden T., Alblas J., Yamamoto M. 3D bioprinting of methacrylated hyaluronic acid (MeHA) hydrogel with intrinsic osteogenicity. PLoS ONE. 2017;12:e0177628. doi: 10.1371/journal.pone.0177628. PubMed DOI PMC
Skardal A., Zhang J., McCoard L., Xu X., Oottamasathien S., Prestwich G. Photocrosslinkable Hyaluronan-Gelatin Hydrogels for Two-Step Bioprinting. Tissue Eng. Part A. 2010;16:2675–2685. doi: 10.1089/ten.tea.2009.0798. PubMed DOI PMC
Sakai S., Ohi H., Taya M. Gelatin/Hyaluronic Acid Content in Hydrogels Obtained through Blue Light-Induced Gelation Affects Hydrogel Properties and Adipose Stem Cell Behaviors. Biomolecules. 2019;9:342. doi: 10.3390/biom9080342. PubMed DOI PMC
Dobos A., Hoorick J.V., Steiger W., Gruber P., Markovic M., Andriotis O., Rohatschek A., Dubruel P., Thurner P., Vlierberghe S.V., et al. Thiol–Gelatin–Norbornene Bioink for Laser-Based High-Definition Bioprinting. Adv. Healthc. Mater. 2019;9:1900752–1900761. doi: 10.1002/adhm.201900752. PubMed DOI
Noh I., Kim N., Tran H., Lee J., Lee C. 3D printable hyaluronic acid-based hydrogel for its potential application as a bioink in tissue engineering. Biomater. Res. 2019;23:3. doi: 10.1186/s40824-018-0152-8. PubMed DOI PMC
Mehrotra S., Melo B., Hirano M., Keung W., Li R., Mandal B., Shin S. Nonmulberry Silk Based Ink for Fabricating Mechanically Robust Cardiac Patches and Endothelialized Myocardium-on-a-Chip Application. Adv. Funct. Mater. 2020;30:1907436. doi: 10.1002/adfm.201907436. PubMed DOI PMC
Petta D., Armiento A., Grijpma D., Alini M., Eglin D., D’Este M. 3D bioprinting of a hyaluronan bioink through enzymatic-and visible light-crosslinking. Biofabrication. 2018;10:044104–044114. doi: 10.1088/1758-5090/aadf58. PubMed DOI
Kajave N., Schmitt T., Nguyen T.U., Kishore V. Dual crosslinking strategy to generate mechanically viable cell-laden printable constructs using methacrylated collagen bioinks. Mater. Sci. Eng. C. 2020;107:110290–110301. doi: 10.1016/j.msec.2019.110290. PubMed DOI PMC
Yu J.H., Fridrikh S.V., Rutledge G.C. The role of elasticity in the formation of electrospun fibers. Polymer. 2006;47:4789–4797. doi: 10.1016/j.polymer.2006.04.050. DOI
Angel Martinez-Ortiz M., Delia Hernandez-Fuentes A., Pimentel-Gonzalez D.J., Campos-Montiel R.G., Vargas-Torres A., Aguirre-Alvarez G. Extraction and characterization of collagen from rabbit skin: Partial characterization. CYTA-J. Food. 2015;13:253–258. doi: 10.1080/19476337.2014.946451. DOI
Yousefi A.M., Smucker B., Naber A., Wyrick C., Shaw C., Bennett K., Szekely S., Focke C., Wood K. Controlling the extrudate swell in melt extrusion additive manufacturing of 3D scaffolds: A designed experiment. J. Biomater. Sci. 2017;29:195–216. doi: 10.1080/09205063.2017.1409022. PubMed DOI
Tanner R. A theory of die-swell. J. Polym. Sci. Part A-2 Polym. Phys. 1970;8:2067–2078. doi: 10.1002/pol.1970.160081203. DOI
Emmermacher J., Spura D., Cziommer J., Kilian D., Wollborn T., Fritsching U., Steingroewer J., Walther T., Gelinsky M., Lode A. Engineering considerations on extrusion-based bioprinting: Interactions of material behavior, mechanical forces and cells in the printing needle. Biofabrication. 2020;12:025022. doi: 10.1088/1758-5090/ab7553. PubMed DOI
Ning L., Yang B., Mohabatpour F., Betancourt N., Sarker M., Papagerakis P., Chen X. Process-induced cell damage: Pneumatic versus screw-driven bioprinting. Biofabrication. 2020;12:025011. doi: 10.1088/1758-5090/ab5f53. PubMed DOI
Mokrejš P., Gál R., Mrázek P. Biotechnology-Based Production of Food Gelatine from Poultry by-Products. Patent number: CZ 307665. 2019 May 16;
Mokrejš P., Mrázek P., Robert R.G., Pavlačková J. Biotechnological Preparation of Gelatines from Chicken Feet. Polymers. 2019;11:1060. doi: 10.3390/polym11061060. PubMed DOI PMC
Gál R., Mokrejš P., Mrázek P., Pavlačková J., Janáčová D., Orsavová J. Chicken Heads as a Promising By-Product for Preparation of Food Gelatins. Molecules. 2020;25:494. doi: 10.3390/molecules25030494. PubMed DOI PMC
Maia J., Carvalho R., Coelho J., Simoes P., Gil M. Insight on the Periodate Oxidation of Dextran and Its Structural Vicissitudes. Polymer. 2011;52:258–265. doi: 10.1016/j.polymer.2010.11.058. DOI
Zhao H., Heindel N. Determination of Degree of Substitution of Formyl Groups in Polyaldehyde Dextran by the Hydroxylamine Hydrochloride Method. Pharm. Res. 1991;8:400–402. doi: 10.1023/A:1015866104055. PubMed DOI
Ouyang L., Yao R., Zhao Y., Sun W. Effect of bioink properties on printability and cell viability for 3D bioplotting of embryonic stem cells. Biofabrication. 2016;8:035020–035033. doi: 10.1088/1758-5090/8/3/035020. PubMed DOI
Chattopadhyay S., Raines R. Collagen-based biomaterilas for wound healing. Biopolymers. 2014;8:821–830. doi: 10.1002/bip.22486. PubMed DOI PMC
Eisenbarth E. Biomaterials for Tissue Engineering. Adv. Eng. Mater. 2007;9:1051–1060. doi: 10.1002/adem.200700287. DOI
Young A.T., White O.C., Daniele M.A. Rheological Properties of Coordinated Physical Gelation and Chemical Crosslinking in Gelatin Methacryloyl (GelMA) Hydrogels. Macromol. Biosci. 2020;20:2000183. doi: 10.1002/mabi.202000183. PubMed DOI PMC
Draye J.P., Delaey B., de Voorde A.V., Bulcke A.V.D., Reu B.D., Schacht E. In vitro and in vivo biocompatibility of dextran dialdehyde cross-linked gelatin hydrogel films. Biomaterials. 1998;19:1677–1687. doi: 10.1016/S0142-9612(98)00049-0. PubMed DOI
Balakrishnan B., Jayakrishnan A. Self-cross-linking biopolymers as injectable in situ forming biodegradable scaffolds. Biomaterials. 2005;26:3941–3951. doi: 10.1016/j.biomaterials.2004.10.005. PubMed DOI
Kristiansen K., Potthast A., Christensen B. Periodate oxidation of polysaccharides for modification of chemical and physical properties. Carbohydr. Res. 2010;345:1264–1271. doi: 10.1016/j.carres.2010.02.011. PubMed DOI
Liu Z., Li Y., Li W., Lian W., Kemell M., Hietala S., Figueiredo P., Li L., Mäkilä E., Ma M., et al. Close-loop dynamic nanohybrids on collagen-ark with in situ gelling transformation capability for biomimetic stage-specific diabetic wound healing. Mater. Horiz. 2019;6:385–393. doi: 10.1039/C8MH01145A. DOI
Nonsuwan P., Matsugami A., Hayashi F., Hyon S.H., Matsumura K. Controlling the degradation of an oxidized dextran-based hydrogel independent of the mechanical properties. Carbohydr. Polym. 2019;204:131–141. doi: 10.1016/j.carbpol.2018.09.081. PubMed DOI
Winter H. Encyclopedia of Materials: Science and Technology. Elsevier; Amsterdam, The Netherlands: 2001. Chapter Physical and Chemical Gelation.
Wu D., Yu Y., Tan J., Huang L., Luo B., Lu L., Zhou C. 3D bioprinting of gellan gum and poly (ethylene glycol) diacrylate based hydrogels to produce human-scale constructs with high-fidelity. Mater. Des. 2018;160:486–495. doi: 10.1016/j.matdes.2018.09.040. DOI
Khorshidi S., Karkhaneh A., Bonakdar S., Omidian M. High-strength functionalized pectin/fibroin hydrogel with tunable properties: A structure–property relationship study. J. Appl. Polym. Sci. 2019;137:48859–48872. doi: 10.1002/app.48859. DOI
Zehnder T., Freund T., Demir M., Detsch R., Boccaccini A. Fabrication of Cell-Loaded Two-Phase 3D Constructs for Tissue Engineering. Materials. 2016;9:887. doi: 10.3390/ma9110887. PubMed DOI PMC
McIlroy C., Olmsted P. Deformation of an amorphous polymer during the fused-filament-fabrication method for additive manufacturing. J. Rheol. 2017;61:379–397. doi: 10.1122/1.4976839. DOI
Comminal R., Serdeczny M., Pedersen D., Spangenberg J. Numerical modeling of the strand deposition flow in extrusion-based additive manufacturing. Addit. Manuf. 2018;20:68–76. doi: 10.1016/j.addma.2017.12.013. DOI
Serdeczny M., Comminal R., Pedersen D., Spangenberg J. Experimental validation of a numerical model for the strand shape in material extrusion additive manufacturing. Addit. Manuf. 2018;24:145–153. doi: 10.1016/j.addma.2018.09.022. DOI
Xia H., Lu J., Tryggvason G. A numerical study of the effect of viscoelastic stresses in fused filament fabrication. Comput. Methods Appl. Mech. Eng. 2019;346:242–259. doi: 10.1016/j.cma.2018.11.031. DOI
Hebda M., McIlroy C., Whiteside B., Caton-Rose F., Coates P. A method for predicting geometric characteristics of polymer deposition during fused-filament-fabrication. Addit. Manuf. 2019;27:99–108. doi: 10.1016/j.addma.2019.02.013. DOI
Coogan T., Kazmer D. Modeling of interlayer contact and contact pressure during fused filament fabrication. J. Rheol. 2019;63:655–672. doi: 10.1122/1.5093033. DOI
Gopi S., Kontopoulou M. Investigation of thermoplastic melt flow and dimensionless groups in 3D bioplotting. Rheol. Acta. 2020;59:83–93. doi: 10.1007/s00397-019-01186-4. DOI
Ahmed E. Hydrogel: Preparation, characterization, and applications. J. Adv. Res. 2015;6:105–121. doi: 10.1016/j.jare.2013.07.006. PubMed DOI PMC
Trautmann A., Rüth M., Lemke H.D., Walther T., Hellmann R. Two-photon polymerization based large scaffolds for adhesion and proliferation studies of human primary fibroblasts. Opt. Laser Technol. 2018;106:474–480. doi: 10.1016/j.optlastec.2018.05.008. DOI
Choksakulnimitr S., Masuda S., Tokuda H., Takakura Y., Hashida M. In vitro cytotoxicity of macromolecules in different cell culture systems. J. Control. Release. 1995;34:233–241. doi: 10.1016/0168-3659(95)00007-U. DOI
Groot C.D., Luyn M.V., Dijk-Wolthuis W.V., Cadee J., Plantinga J., Otter W.D., Hennink W. In vitro biocompatibility of biodegradable dextran-based hydrogels tested with human fibroblasts. Biomaterials. 2001;22:1197–1203. doi: 10.1016/S0142-9612(00)00266-0. PubMed DOI
Poursamar S., Hatami J., Lehner A., da Silva C., Ferreira F., Antunes A. Gelatin porous scaffolds fabricated using a modified gas foaming technique: Characterisation and cytotoxicity assessment. Mater. Sci. Eng. C. 2015;48:63–70. doi: 10.1016/j.msec.2014.10.074. PubMed DOI
Pronina E., Vorotnikov Y., Pozmogova T., Solovieva A., Miroshnichenko S., Plyusnin P., Pishchur D., Eltsov I., Edeleva M., Efremova M.S.O. No Catalyst Added Hydrogen Peroxide Oxidation of Dextran: An Environmentally Friendly Route to Multifunctional Polymers. ACS Sustain. Chem. Eng. 2020;8:5371–5379. doi: 10.1021/acssuschemeng.0c01030. DOI
Artzi N., Shazly T., Crespo C., Ramos A., Chenault H., Edelman E. Characterization of Star Adhesive Sealants Based on PEG/Dextran Hydrogels. Macromol. Biosci. 2009;9:754–765. doi: 10.1002/mabi.200800355. PubMed DOI PMC