Synthesis and Exfoliation of Calcium Organophosphonates for Tailoring Rheological Properties of Sodium Alginate Solutions: A Path toward Polysaccharide-Based Bioink
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
37249916
PubMed Central
PMC10336848
DOI
10.1021/acs.biomac.3c00081
Knihovny.cz E-resources
- MeSH
- Printing, Three-Dimensional MeSH
- Alginates chemistry MeSH
- Bioprinting * methods MeSH
- Hydrogels pharmacology chemistry MeSH
- Mice MeSH
- Organophosphonates * MeSH
- Polymers MeSH
- Rheology MeSH
- Tissue Engineering methods MeSH
- Tissue Scaffolds chemistry MeSH
- Calcium MeSH
- Animals MeSH
- Check Tag
- Mice MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Alginates MeSH
- Hydrogels MeSH
- Organophosphonates * MeSH
- Polymers MeSH
- Calcium MeSH
Layered nanoparticles with surface charge are explored as rheological modifiers for extrudable materials, utilizing their ability to induce electrostatic repulsion and create a house-of-cards structure. These nanoparticles provide mechanical support to the polymer matrix, resulting in increased viscosity and storage modulus. Moreover, their advantageous aspect ratio allows for shear-induced orientation and decreased viscosity during flow. In this work, we present a synthesis and liquid-based exfoliation procedure of phenylphosphonate-phosphate particles with enhanced ability to be intercalated by hydrophilic polymers. These layered nanoparticles are then tested as rheological modifiers of sodium alginate. The effective rheological modification is proved as the viscosity increases from 101 up to 103 Pa·s in steady state. Also, shear-thinning behavior is observed. The resulting nanocomposite hydrogels show potential as an extrudable bioink for 3D printing in tissue engineering and other biomedical applications, with good shape fidelity, nontoxicity, and satisfactory cell viability confirmed through encapsulation and printing of mouse fibroblasts.
Lehrstuhl Biomaterialien Universitat Bayreuth Prof Rudiger Bormann Strasse 1 95447 Bayreuth Germany
National Institute of Rheumatic Diseases Nabrezie 1 Krasku 4 921 12 Piestany Slovak Republic
Polymer Institute of Slovak academy of Sciences Dubravska cesta 9 84541 Bratislava Slovak Republic
See more in PubMed
Li J.; Wu C. T.; Chu P. K.; Gelinsky M. 3D printing of hydrogels: Rational design strategies and emerging biomedical applications. Mater. Sci. Eng. R Rep. 2020, 140, 100543.10.1016/j.mser.2020.100543. DOI
Benwood C.; Chrenek J.; Kirsch R. L.; Masri N. Z.; Richards H.; Teetzen K.; Willerth S. M. Natural Biomaterials and Their Use as Bioinks for Printing Tissues. Bioeng. 2021, 8 (2), 27.10.3390/bioengineering8020027. PubMed DOI PMC
Wu X.; Li W.; Chen K.; Zhang D. K.; Xu L. M.; Yang X. H. A tough PVA/HA/COL composite hydrogel with simple process and excellent mechanical properties. Mater. Today Commun. 2019, 21, 100702.10.1016/j.mtcomm.2019.100702. DOI
Zhu H.; Monavari M.; Zheng K.; Distler T.; Ouyang L. L.; Heid S.; Jin Z. R.; He J. K.; Li D. C.; Boccaccini A. R. 3D Bioprinting of Multifunctional Dynamic Nanocomposite Bioinks Incorporating Cu-Doped Mesoporous Bioactive Glass Nanoparticles for Bone Tissue Engineering. Small 2022, 18 (12), 2104996.10.1002/smll.202104996. PubMed DOI
Karis D.; Nelson A. Time-dependent covalent network formation in extrudable hydrogels. Polym. Chem. 2020, 11 (43), 6910–6918. 10.1039/D0PY01129K. DOI
Li Z. W.; Du T. M.; Ruan C. S.; Niu X. F. Bioinspired mineralized collagen scaffolds for bone tissue engineering. Bioact. Mater. 2021, 6 (5), 1491–1511. 10.1016/j.bioactmat.2020.11.004. PubMed DOI PMC
Lee A.; Hudson A. R.; Shiwarski D. J.; Tashman J. W.; Hinton T. J.; Yerneni S.; Bliley J. M.; Campbell P. G.; Feinberg A. W. 3D bioprinting of collagen to rebuild components of the human heart. Science 2019, 365 (6452), 482.10.1126/science.aav9051. PubMed DOI
Dutta S. D.; Hexiu J.; Patel D. K.; Ganguly K.; Lim K. T. 3D-printed bioactive and biodegradable hydrogel scaffolds of alginate/gelatin/cellulose nanocrystals for tissue engineering. Int. J. Biol. Macromol. 2021, 167, 644–658. 10.1016/j.ijbiomac.2020.12.011. PubMed DOI
Gao F.; Xu Z. Y.; Liang Q. F.; Li H. F.; Peng L. Q.; Wu M. M.; Zhao X. L.; Cui X.; Ruan C. S.; Liu W. G. Osteochondral Regeneration with 3D-Printed Biodegradable High-Strength Supramolecular Polymer Reinforced-Gelatin Hydrogel Scaffolds. Adv. Sci. 2019, 6 (15), 1900867.10.1002/advs.201900867. PubMed DOI PMC
Sultan S.; Mathew A. P. 3D printed scaffolds with gradient porosity based on a cellulose nanocrystal hydrogel. Nanoscale 2018, 10 (9), 4421–4431. 10.1039/C7NR08966J. PubMed DOI
Bello A. B.; Kim D.; Kim D.; Park H.; Lee S. H. Engineering and Functionalization of Gelatin Biomaterials: From Cell Culture to Medical Applications. Tissue Eng. Part B Rev. 2020, 26 (2), 164–180. 10.1089/ten.teb.2019.0256. PubMed DOI
Anand R.; Amoli M. S.; Huysecom A. S.; Amorim P. A.; Agten H.; Geris L.; Bloemen V. A tunable gelatin-hyaluronan dialdehyde/methacryloyl gelatin interpenetrating polymer network hydrogel for additive tissue manufacturing. Biomed. Mater. 2022, 17 (4), 045027.10.1088/1748-605X/ac78b8. PubMed DOI
Kim H. S.; Kim C.; Lee K. Y. Three-dimensional bioprinting of polysaccharide-based self-healing hydrogels with dual cross-linking. J. Biomed. Mater. Res., Part A 2022, 110 (4), 761–772. 10.1002/jbm.a.37325. PubMed DOI
Roh H. K.; Kim H. S.; Kim C.; Lee K. Y. 3D Printing of Polysaccharide-Based Self-Healing Hydrogel Reinforced with Alginate for Secondary Cross-Linking. Biomedicines 2021, 9 (9), 1224.10.3390/biomedicines9091224. PubMed DOI PMC
Rastogi P.; Kandasubramanian B. Review of alginate-based hydrogel bioprinting for application in tissue engineering. Biofabrication 2019, 11 (4), 042001.10.1088/1758-5090/ab331e. PubMed DOI
Raus R. A.; Nawawi W. M. F. W.; Nasaruddin R. R. Alginate and alginate composites for biomedical applications. Asian J. Pharm. Sci. 2021, 16 (3), 280–306. 10.1016/j.ajps.2020.10.001. PubMed DOI PMC
Jejurikar A.; Lawrie G.; Martin D.; Grondahl L. A novel strategy for preparing mechanically robust ionically cross-linked alginate hydrogels. Biomed. Mater. 2011, 6 (2), 025010.10.1088/1748-6041/6/2/025010. PubMed DOI
Tam S. K.; Dusseault J.; Bilodeau S.; Langlois G.; Halle J. P.; Yahia L. Factors influencing alginate gel biocompatibility. J. Biomed. Mater. Res., Part A 2011, 98A (1), 40–52. 10.1002/jbm.a.33047. PubMed DOI
Cross L. M.; Shah K.; Palani S.; Peak C. W.; Gaharwar A. K. Gradient nanocomposite hydrogels for interface tissue engineering. Nanomedicine: NBM 2018, 14 (7), 2465–2474. 10.1016/j.nano.2017.02.022. PubMed DOI PMC
Plaizier-Vercammen J. Rheological properties of Laponite® XLG, a synthetic purified hectorite. Pharmazie 1992, 47 (11), 856–861.
Afghah F.; Altunbek M.; Dikyol C.; Koc B. Preparation and characterization of nanoclay-hydrogel composite support-bath for bioprinting of complex structures. Sci. Rep. 2020, 10 (1), 5257.10.1038/s41598-020-61606-x. PubMed DOI PMC
Reich H.; Dijkstra M.; van Roij R.; Schmidt M. Entropic Wetting and the Free Isotropic-Nematic Interface of Hard Colloidal Platelets. J. Phys. Chem. B 2007, 111 (27), 7825–7835. 10.1021/jp068870b. PubMed DOI
Davila J. L.; dÁvila M. A. Laponite® as a rheology modifier of alginate solutions: Physical gelation and aging evolution. Carbohydr. Polym. 2017, 157, 1–8. 10.1016/j.carbpol.2016.09.057. PubMed DOI
Davila J. L.; dÁvila M. A. Rheological evaluation of Laponite®/alginate inks for 3D extrusion-based printing. J. Adv. Manuf. Technol. 2019, 101, 675–686. 10.1007/s00170-018-2876-y. DOI
Leu A. R.; Cucuruz A.; Ghitulica C. D.; Voicu G.; Stamat L. R.; Dinescu S.; Vlasceanu G. M.; Stavarache C.; Ianchis R.; Iovu H. 3D Printable Composite Biomaterials Based on GelMA and Hydroxyapatite Powders Doped with Cerium Ions for Bone Tissue Regeneration. Int. J. Mol. Sci. 2022, 23 (3), 1841.10.3390/ijms23031841. PubMed DOI PMC
Teepakakorn A.; Ogawa M. Interactions of layered clay minerals with water-soluble polymers; structural design and functions. Appl. Clay Sci. 2022, 222, 106487.10.1016/j.clay.2022.106487. DOI
Haraguchi K.; Farnworth R.; Ohbayashi A.; Takehisa T. Compositional Effects on Mechanical Properties of Nanocomposite Hydrogels Composed of Poly(N, N-dimethylacrylamide) and Clay. Macromolecules 2003, 36 (15), 5732–5741. 10.1021/ma034366i. DOI
Patarroyo J. L.; Cifuentes J.; Munoz L. N.; Cruz J. C.; Reyes L. H. Novel antibacterial hydrogels based on gelatin/polyvinyl-alcohol and graphene oxide/silver nanoconjugates: formulation, characterization, and preliminary biocompatibility evaluation. Heliyon 2022, 8 (3), e09145.10.1016/j.heliyon.2022.e09145. PubMed DOI PMC
Paydayesh A.; Heleil L.; Sh A. D. Preparation and application of poly(hydroxyl ethyl methacrylate) nanocomposite hydrogels containing iron oxide nanoparticles as wound dressing. Polym. Polym. Compos. 2022, 30, 09673911211063106.10.1177/09673911211063106. DOI
Fang Z.; Qiao K.; Wang Y. S.; Zheng Y. D.; He W.; Xie Y. J.; Yang H. Y. Injectable and biodegradable double-network nanocomposite hydrogel with regulable sol-gel transition process and mechanical properties. Polym. Test. 2022, 106, 107452.10.1016/j.polymertesting.2021.107452. DOI
Saglam-Metiner P.; Gulce-Iz S.; Biray-Avci C. Bioengineering-inspired three-dimensional culture systems: Organoids to create tumor microenvironment. Gene 2019, 686, 203–212. 10.1016/j.gene.2018.11.058. PubMed DOI
Jung G. Y.; Park Y. J.; Han J. S. Effects of HA released calcium ion on osteoblast differentiation. J. Mater. Sci.: Mater. Med. 2010, 21 (5), 1649–1654. 10.1007/s10856-010-4011-y. PubMed DOI
Beck G. Inorganic phosphate regulates multiple genes during osteoblast differentiation, including Nrf2. Exp. Cell Res. 2003, 288 (2), 288–300. 10.1016/S0014-4827(03)00213-1. PubMed DOI
Fischer L.; Nosratlo M.; Hast K.; Karakaya E.; Strohlein N.; Esser T. U; Gerum R.; Richter S.; Engel F B; Detsch R.; Fabry B.; Thievessen I. Calcium supplementation of bioinks reduces shear stress-induced cell damage during bioprinting. Biofabrication 2022, 14 (4), 045005.10.1088/1758-5090/ac84af. PubMed DOI
Ribeiro A.; Blokzijl M. M.; Levato R.; Visser C. W.; Castilho M.; Hennink W. E.; Vermonden T.; Malda J. Assessing bioink shape fidelity to aid material development in 3D bioprinting. Biofabrication 2018, 10 (1), 014102.10.1088/1758-5090/aa90e2. PubMed DOI PMC
Klapetek P., Necas D., Anderson C. “Gwyddion - Free SPM data analysis software”, v. 2.53, 2019.
Sahoo P. K.; Soltani S.; Wong A. K. C. A survey of thresholding techniques. Comput. graph. image process. 1988, 41 (2), 233–260. 10.1016/0734-189X(88)90022-9. DOI
Knotek P.; Vlcek M.; Kincl M.; Tichy L. On the ultraviolet light induced oxidation of amorphous As2S3 film. Thin Solid Films 2012, 520 (16), 5472–5478. 10.1016/j.tsf.2012.03.116. DOI
Knotek P.; Tichy L. Atomic force microscopy and atomic force acoustic microscopy characterization of photo-induced changes in some Ge-As-S amorphous films. Thin Solid Films 2009, 517 (5), 1837–1840. 10.1016/j.tsf.2008.09.041. DOI
Svoboda J.; Zima V.; Benes L.; Melanova K.; Vicek M. Synthesis and Characterization of New Calcium Phenylphosphonates and 4-Carboxyphenylphosphonates. Inorg. Chem. 2005, 44 (26), 9968–9976. 10.1021/ic051606x. PubMed DOI
Kopecka K.; Benes L.; Melanova K.; Zima V.; Knotek P.; Zetkova K. Layered calcium phenylphosphonate: a hybrid material for a new generation of nanofillers. Beilstein J. Nanotechnol. 2018, 9, 2906–2915. 10.3762/bjnano.9.269. PubMed DOI PMC
Sevrain C. M.; Berchel M.; Couthon H.; Jaffres P. A. Phosphonic acid: preparation and applications. Beilstein J. Org. Chem. 2017, 13, 2186–2213. 10.3762/bjoc.13.219. PubMed DOI PMC
Vandecandelaere N.; Rey C.; Drouet C. Biomimetic apatite-based biomaterials: on the critical impact of synthesis and post-synthesis parameters. J. Mater. Sci.: Mater. Med. 2012, 23 (11), 2593–2606. 10.1007/s10856-012-4719-y. PubMed DOI
Niu L.; Coleman J. N.; Zhang H.; Shin H.; Chhowalla M.; Zheng Z. J. Production of Two-Dimensional Nanomaterials via Liquid-Based Direct Exfoliation. Small 2016, 12 (3), 272–293. 10.1002/smll.201502207. PubMed DOI
Coleman J. N.; Lotya M.; O’Neill A.; Bergin S. D.; King P. J.; Khan U.; Young K.; Gaucher A.; De S.; Smith R. J.; Shvets I. V.; Arora S. K.; Stanton G.; Kim H.-Y.; Lee K.; Kim G. T.; Duesberg G. S.; Hallam T.; Boland J. J.; Wang J. J.; Donegan J. F.; Grunlan J. C.; Moriarty G.; Shmeliov A.; Nicholls R. J.; Perkins J. M.; Grieveson E. M.; Theuwissen K.; McComb D. W.; Nellist P. D.; Nicolosi V. Two-Dimensional Nanosheets Produced by Liquid Exfoliation of Layered Materials. Science 2011, 331 (6017), 568–571. 10.1126/science.1194975. PubMed DOI
McMartin K. E.; Cenac T. A. Toxicity of Ethylene Glycol Metabolites in Normal Human Kidney Cells. Ann. N. Y. Acad. Sci. 2000, 919 (1), 315–317. 10.1111/j.1749-6632.2000.tb06894.x. PubMed DOI
Fu Z. Q.; Naghieh S.; Xu C. C.; Wang C. J.; Sun W.; Chen X. B. Printability in extrusion bioprinting. Biofabrication 2021, 13 (3), 033001.10.1088/1758-5090/abe7ab. PubMed DOI
Voo V. P.; Ooi C. W.; Islam A.; Tey B. T.; Chan E. S. Calcium alginate hydrogel beads with high stiffness and extended dissolution behaviour. Eur. Polym. J. 2016, 75, 343–353. 10.1016/j.eurpolymj.2015.12.029. 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 (3), 035020.10.1088/1758-5090/8/3/035020. PubMed DOI
Zhang M.; Vora A.; Han W.; Wojtecki R. J.; Maune H.; Le A. B. A.; Thompson L. E.; McClelland G. M.; Ribet F.; Engler A. C.; Nelson A. Dual-Responsive Hydrogels for Direct-Write 3D Printing. Macromolecules 2015, 48 (18), 6482–6488. 10.1021/acs.macromol.5b01550. DOI
Hölzl K.; Lin S. M.; Tytgat L.; Van Vlierberghe S.; Gu L. X.; Ovsianikov A. Bioink properties before, during and after 3D bioprinting. Biofabrication 2016, 8 (3), 032002.10.1088/1758-5090/8/3/032002. PubMed DOI
Gillispie G.; Prim P.; Copus J.; Fisher J.; Mikos A. G.; Yoo J. J.; Atala A.; Lee S. J. Assessment methodologies for extrusion-based bioink printability. Biofabrication 2020, 12 (2), 022003.10.1088/1758-5090/ab6f0d. PubMed DOI PMC
Wang K.4. Die Swell of Complex Polymeric Systems. In Viscoelasticity - From Theory to Biological Applications; De Vicente J., Ed.; InTechOpen: 2012. .
Metzner A. B. Rheology of Suspensions in Polymeric Liquids. J. Rheol. 1985, 29 (6), 739–775. 10.1122/1.549808. DOI
Stabik J. Influence of Filler Particle Geometry on Die Swell. Int. Polym. Process. 2004, 19 (4), 350–355. 10.3139/217.1840. DOI
Olderøy M. Ø.; Xie M.; Andreassen J.-P.; Strand B. L.; Zhang Z.; Sikorski P. Viscoelastic properties of mineralized alginate hydrogel beads. J. Mater. Sci.: Mater. Med. 2012, 23 (7), 1619–1627. 10.1007/s10856-012-4655-x. PubMed DOI
Serrano-Aroca A.; Ruiz-Pividal J. F.; Llorens-Gámez M. Enhancement of water diffusion and compression performance of crosslinked alginate films with a minuscule amount of graphene oxide. Sci. Rep. 2017, 7, 11684.10.1038/s41598-017-10260-x. PubMed DOI PMC
Qin Y. Gel swelling properties of alginate fibers. J. Appl. Polym. Sci. 2004, 91 (3), 1641–1645. 10.1002/app.13317. DOI
Bajpai S.K.; Sharma S. Investigation of swelling/degradation behaviour of alginate beads crosslinked with Ca2+ and Ba2+ ions. React. Funct. Polym. 2004, 59 (2), 129–140. 10.1016/j.reactfunctpolym.2004.01.002. DOI
Matyash M.; Despang F.; Ikonomidou C.; Gelinsky M. Swelling and Mechanical Properties of Alginate Hydrogels with Respect to Promotion of Neural Growth. Tissue Eng., Part C 2014, 20 (5), 401–411. 10.1089/ten.tec.2013.0252. PubMed DOI
Donati I.; et al. New Hypothesis on the Role of Alternating Sequences in Calcium-Alginate Gels. Biomacromolecules 2005, 6 (2), 1031–1040. 10.1021/bm049306e. PubMed DOI
Garland E. M.; Parr J. M.; Williamson D. S.; Cohen S. M. In vitro cytotoxicity of the sodium, potassium and calcium salts of saccharin, sodium ascorbate, sodium citrate and sodium chloride. Toxicol. In Vitro 1989, 3 (3), 201–205. 10.1016/0887-2333(89)90006-4. PubMed DOI
Soltan N.; Ning L. Q.; Mohabatpour F.; Papagerakis P.; Chen X. B. Printability and Cell Viability in Bioprinting Alginate Dialdehyde-Gelatin Scaffolds. ACS Biomater. Sci. Eng. 2019, 5 (6), 2976–2987. 10.1021/acsbiomaterials.9b00167. PubMed DOI
Blaeser A.; Duarte Campos D. F.; Puster U.; Richtering W.; Stevens M. M.; Fischer H. Controlling Shear Stress in 3D Bioprinting is a Key Factor to Balance Printing Resolution and Stem Cell Integrity. Adv. Healthcare Mater. 2016, 5 (3), 326–333. 10.1002/adhm.201500677. PubMed DOI
Lemarié L.; Anandan A.; Petiot E.; Marquette C.; Courtial E. J. Rheology, simulation and data analysis toward bioprinting cell viability awareness. Bioprinting 2021, 21, e00119.10.1016/j.bprint.2020.e00119. DOI
Roquero D. M.; Othman A.; Melman A.; Katz E. Iron (III)-cross-linked alginate hydrogels: a critical review. Mater. Adv. 2022, 3 (4), 1849–1873. 10.1039/D1MA00959A. DOI
Hotchkiss P. J.; Jones S. C.; Paniagua S. A.; Sharma A.; Kippelen B.; Armstrong N. R.; Marder S. R. The Modification of Indium Tin Oxide with Phosphonic Acids: Mechanism of Binding, Tuning of Surface Properties, and Potential for Use in Organic Electronic Applications. Acc. Chem. Res. 2012, 45 (3), 337–346. 10.1021/ar200119g. PubMed DOI
Kato M.; Makino S.; Kimura H.; Ota T.; Furuhashi T.; Nagamura Y. Evaluation of mitochondrial function and membrane integrity by dual fluorescent staining for assessment of sperm status in rats. J. Toxicol. Sci. 2002, 27 (1), 11–19. 10.2131/jts.27.11. PubMed DOI
Lechner A.; Trossmann V. T.; Scheibel T. Impact of Cell Loading of Recombinant Spider Silk Based Bioinks on Gelation and Printability. Macromol. Biosci. 2022, 22 (3), 2100390.10.1002/mabi.202100390. PubMed DOI