Acrylamide-based hydrogels with distinct osteogenic and chondrogenic differentiation potential
- School of Pharmacy and Bioengineering, Keele University, Keele, GB Department of Clinical Laboratory Sciences, College of Pharmacy, University of Mosul, Mosul, IQ
- Department of Chemistry, School of Science, Loughborough University, Leicestershire, GB
- School of Pharmacy and Bioengineering, Keele University, Keele, GB
Published in Issue 2022-07-16
How to Cite
Younus, Z. M., Roach, P., & Forsyth, N. R. (2022). Acrylamide-based hydrogels with distinct osteogenic and chondrogenic differentiation potential. Progress in Biomaterials, 11(3 (September 2022). https://doi.org/10.1007/s40204-022-00196-5
Abstract
Abstract Regeneration solutions for the osteochondral interface depth are limited, where multi-material implants have the potential to delaminate affecting the regeneration process and impacting the final integrity of tissue interface. Here we explore regionally mixed hydrogel networks, presenting distinct chemical features to determine their compatibility in supporting osteogenic or chondrogenic cell behaviour and differentiation. Poly( N -isopropylacrylamide) (pNIPAM) and poly( N - tert -butylacrylamide) (pNTBAM) hydrogels were assessed in terms of their chemical differences, mechanical strength, internal architecture, porosity and capacity to support cell viability, migration, and differentiation. pNTBAM polymerized with a Young’s modulus of up to 371 ± 31 kPa compared to the more flexible pNIPAM, 16.5 ± 0.6 kPa. Viability testing revealed biocompatibility of both hydrogels with significantly increased cell numbers observed in pNTBAM (500 ± 95 viable cells/mm 2 ) than in pNIPAM (60 ± 3 viable cells/mm 2 ) ( P ≤ 0.05). Mineralization determined through alkaline phosphatase (ALP) activity, calcium ion and annexin A2 markers of mineralization) and osteogenic behaviour (collagen I expression) were supported in both hydrogels, but to a greater extent in pNTBAM. pNTBAM supported significantly elevated levels of chondrogenic markers as evidenced by collagen II and glycosaminoglycan expression in comparison to little or no evidence in pNIPAM ( P ≤ 0.05). In conclusion, structurally similar, chemically distinct, acrylamide hydrogels display variable capacities in supporting osteochondral cell behaviours. These systems demonstrate spatial control of cell interaction through simple changes in monomer chemistry. Fine control over chemical presentation during the fabrication of biomaterial implants could lead to greater efficacy and targeted regeneration of semi-complex tissues.Keywords
- Hydrogel,
- Osteochondral,
- Osteogenic,
- Chondrogenic,
- Mineralization
References
- Bian et al. (2016) Morphological characteristics of cartilage-bone transitional structures in the human knee joint and CAD design of an osteochondral scaffold (pp. 1-14) https://doi.org/10.1186/s12938-016-0200-3
- Camarero-Espinosa and Cooper-White (2017) Tailoring biomaterial scaffolds for osteochondral repair (pp. 476-489) https://doi.org/10.1016/j.ijpharm.2016.10.035
- Cha et al. (2011) Tuning the dependency between stiffness and permeability of a cell encapsulating hydrogel with hydrophilic pendant chains 7(10) (pp. 3719-3728) https://doi.org/10.1016/j.actbio.2011.06.017
- Chang and Wang (2011) Cell responses to surface and architecture of tissue engineering scaffolds https://doi.org/10.5772/21983
- Chen et al. (2018) Tuning surface properties of bone biomaterials to manipulate osteoblastic cell adhesion and the signaling pathways for the enhancement of early osseointegration (pp. 58-69) https://doi.org/10.1016/j.colsurfb.2018.01.022
- Cooper et al. (2016) Cortical bone porosity: what is it, why is it important, and how can we detect it? 14(5) (pp. 187-198) https://doi.org/10.1007/s11914-016-0319-y
- Dale et al. (2015) Immortalisation with hTERT impacts on sulphated glycosaminoglycan secretion and immunophenotype in a variable and cell specific manner https://doi.org/10.1371/journal.pone.0133745
- Di Luca et al. (2015) The osteochondral interface as a gradient tissue: from development to the fabrication of gradient scaffolds for regenerative medicine 105(1) (pp. 34-52) https://doi.org/10.1002/bdrc.21092
- Di Luca et al. (2016) Gradients in pore size enhance the osteogenic differentiation of human mesenchymal stromal cells in three-dimensional scaffolds 6(March) (pp. 1-13) https://doi.org/10.1038/srep22898
- Di Luca et al. (2016) Influencing chondrogenic differentiation of human mesenchymal stromal cells in scaffolds displaying a structural gradient in pore size (pp. 210-219) https://doi.org/10.1016/J.ACTBIO.2016.03.014
- Engler et al. (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments 166(6) (pp. 877-887) https://doi.org/10.1083/jcb.200405004
- Engler et al. (2006) Matrix elasticity directs stem cell lineage specification 126(4) (pp. 677-689) https://doi.org/10.1016/J.CELL.2006.06.044
- Ermis et al. (2018) Micro and Nanofabrication methods to control cell-substrate interactions and cell behavior: a review from the tissue engineering perspective 3(3) (pp. 355-369) https://doi.org/10.1016/j.bioactmat.2018.05.005
- Fang et al. (2019) A strong, tough, and osteoconductive hydroxyapatite mineralized polyacrylamide/dextran hydrogel for bone tissue regeneration (pp. 503-513) https://doi.org/10.1016/J.ACTBIO.2019.02.019
- Farndale et al. (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue 883(2) (pp. 173-177) https://doi.org/10.1016/0304-4165(86)90306-5
- Flemming et al. (1999) Effects of synthetic micro-and nano-structured surfaces on cell behavior 20(1999) (pp. 573-588) https://doi.org/10.1016/S0142-9612(98)00209-9
- Franz et al. (2001) In situ compressive stiffness, biochemical composition, and structural integrity of articular cartilage of the human knee joint 9(6) (pp. 582-592) https://doi.org/10.1053/joca.2001.0418
- Gajendiran et al. (2017) Conductive biomaterials for tissue engineering applications (pp. 12-26) https://doi.org/10.1016/j.jiec.2017.02.031
- Griffon et al. (2006) Chitosan scaffolds: interconnective pore size and cartilage engineering 2(3) (pp. 313-320) https://doi.org/10.1016/j.actbio.2005.12.007
- Helgeland et al. (2021) Dual-crosslinked 3D printed gelatin scaffolds with potential for temporomandibular joint cartilage regeneration 16(3) https://doi.org/10.1088/1748-605X/ABE6D9
- Hoffman (2012) Hydrogels for biomedical applications (pp. 18-23) https://doi.org/10.1016/j.addr.2012.09.010
- Hutmacher (2001) Scaffold design and fabrication technologies for engineering tissues — state of the art and future perspectives 12(1) (pp. 107-124) https://doi.org/10.1163/156856201744489
- Izadifar et al. (2012) Strategic Design and fabrication of engineered scaffolds for articular cartilage repair 3(4) (pp. 799-838) https://doi.org/10.3390/jfb3040799
- Jin et al. (2019) Osteochondral tissue regenerated via a strategy by stacking pre-differentiated BMSC sheet on fibrous mesh in a gradient 14(6) https://doi.org/10.1088/1748-605X/AB49E2
- Jones (2015) Reprint of: review of bioactive glass: From Hench to hybrids (pp. S53-S82) https://doi.org/10.1016/j.actbio.2015.07.019
- Karageorgiou and Kaplan (2005) Porosity of 3D biomaterial scaffolds and osteogenesis 26(27) (pp. 5474-5491) https://doi.org/10.1016/j.biomaterials.2005.02.002
- Khoryani et al. (2018) Investigating the effects of polymer molecular weight and non-solvent content on the phase separation, surface morphology and hydrophobicity of polyvinyl chloride films (pp. 933-940) https://doi.org/10.1016/j.apsusc.2017.09.235
- Lee et al. (2012) Potential bone replacement materials prepared by two methods https://doi.org/10.1557/opl.2012.671
- Lien et al. (2009) Effect of pore size on ECM secretion and cell growth in gelatin scaffold for articular cartilage tissue engineering 5(2) (pp. 670-679) https://doi.org/10.1016/j.actbio.2008.09.020
- Little et al. (2011) Mechanical properties of natural cartilage and tissue-engineered constructs 17(4) (pp. 213-227) https://doi.org/10.1089/ten.teb.2010.0572
- Lynch et al. (2005) Correlation of the adhesive properties of cells to N -Isopropylacrylamide / N - tert -Butylacrylamide copolymer surfaces with changes in surface structure using contact angle measurements, molecular simulations, and Raman Spectroscopy 17(6) (pp. 3889-3898) https://doi.org/10.1021/cm0506959
- Malafaya and Reis (2009) Bilayered chitosan-based scaffolds for osteochondral tissue engineering: Influence of hydroxyapatite on in vitro cytotoxicity and dynamic bioactivity studies in a specific double-chamber bioreactor 5(2) (pp. 644-660) https://doi.org/10.1016/j.actbio.2008.09.017
- Matyjaszewski (2012) Atom transfer radical polymerization (ATRP): current status and future perspectives 45(10) (pp. 4015-4039) https://doi.org/10.1021/ma3001719
- Morin (1974) Direct colorimetric determination of serum calcium with o cresolphthalein complexion 61(1) (pp. 114-117) https://doi.org/10.1093/ajcp/61.1.114
- Murphy et al. (2010) The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering 31(3) (pp. 461-466) https://doi.org/10.1016/j.biomaterials.2009.09.063
- Nam and Park (1999) Porous biodegradable polymeric scaffolds prepared by thermally induced phase separation 47(1) (pp. 8-17) https://doi.org/10.1002/(SICI)1097-4636(199910)47:1<8::AID-JBM2>3.0.CO;2-L
- Nukavarapu and Dorcemus (2013) Osteochondral tissue engineering: current strategies and challenges 31(5) (pp. 706-721) https://doi.org/10.1016/j.biotechadv.2012.11.004
- Pal (2014) Design of artificial human joints & organs (pp. 1-419) https://doi.org/10.1007/978-1-4614-6255-2
- Qavi et al. (2014) Acrylamide hydrogels preparation via free radical crosslinking copolymerization: kinetic study and morphological investigation 51(10) (pp. 842-848) https://doi.org/10.1080/10601325.2014.937132
- Remanan et al. (2018) Recent advances in preparation of porous polymeric membranes by unique techniques and mitigation of fouling through surface modification 3(2) (pp. 609-633) https://doi.org/10.1002/slct.201702503
- Rzaev et al. (2007) Functional copolymers of N-isopropylacrylamide for bioengineering applications 32(5) (pp. 534-595) https://doi.org/10.1016/j.progpolymsci.2007.01.006
- Sobral et al. (2011) Three-dimensional plotted scaffolds with controlled pore size gradients: effect of scaffold geometry on mechanical performance and cell seeding efficiency 7(3) (pp. 1009-1018) https://doi.org/10.1016/j.actbio.2010.11.003
- Tan et al. (2005) Improved cell adhesion and proliferation on synthetic phosphonic acid-containing hydrogels 26(17) (pp. 3663-3671) https://doi.org/10.1016/j.biomaterials.2004.09.053
- Turnbull et al. (2018) 3D bioactive composite scaffolds for bone tissue engineering 3(3) (pp. 278-314) https://doi.org/10.1016/j.bioactmat.2017.10.001
- Wan et al. (2005) Adhesion and proliferation of OCT-1 osteoblast-like cells on micro- and nano-scale topography structured poly(L-lactide) 26(21) (pp. 4453-4459) https://doi.org/10.1016/j.biomaterials.2004.11.016
- Wells (2008) The role of matrix stiffness in regulating cell behavior 47(4) (pp. 1394-1400) https://doi.org/10.1002/hep.22193
- Yang et al. (2017) Cell-laden hydrogels for osteochondral and cartilage tissue engineering (pp. 1-25) https://doi.org/10.1016/j.actbio.2017.01.036
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