Binary phase solid-state photopolymerization of acrylates: design, characterization and biomineralization of 3D scaffolds for tissue engineering

doi:10.1007/s11706-017-0394-8

Front. Mater. Sci.

2017, Vol. 11

Issue (4) : 307-317 https://doi.org/10.1007/s11706-017-0394-8

RESEARCH ARTICLE

Binary phase solid-state photopolymerization of acrylates: design, characterization and biomineralization of 3D scaffolds for tissue engineering

Inamullah MAITLO, Safdar ALI, Muhammad Yasir AKRAM, Farooq Khurum SHEHZAD, Jun NIE(

)

State Key Laboratory of Chemical Resource Engineering & Beijing Laboratory of Biomedical Materials, Beijing University of Chemical Technology, Beijing 100029, China

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Abstract

Porous polymer scaffolds designed by the cryogel method are attractive materials for a range of tissue engineering applications. However, the use of toxic cross-linker for retaining the pore structure limits their clinical applications. In this research, acrylates (HEA/PEGDA, HEMA/PEGDA and PEGDA) were used in the low-temperature soli d-state photopolymerization to produce porous scaffolds with good structural retention. The morphology, pore diameter, mineral deposition and water absorption of the scaffold were characterized by SEM and water absorption test respectively. Elemental analysis and cytotoxicity of the biomineralized scaffold were revealed by using XRD and MTT assay test. The PEGDA-derived scaffold showed good water absorption ability and a higher degree of porosity with larger pore size compared to others. XRD patterns and IR results confirmed the formation of hydroxyapatite crystals from an alternative socking process. The overall cell proliferation was excellent, where PEGDA-derived scaffold had the highest and the most uniform cell growth, while HEMA/PEGDA scaffold showed the least. These results suggest that the cell proliferation and adhesion are directly proportional to the pore size, the shape and the porosity of scaffolds.

Keywords binary phase solid-state photopolymerization phase separation tissue engineering biomineralization MTT

Corresponding Author(s): Jun NIE

Online First Date: 29 September 2017 Issue Date: 29 November 2017

Cite this article:

Inamullah MAITLO,Safdar ALI,Muhammad Yasir AKRAM, et al. Binary phase solid-state photopolymerization of acrylates: design, characterization and biomineralization of 3D scaffolds for tissue engineering[J]. Front. Mater. Sci., 2017, 11(4): 307-317.

URL:

https://academic.hep.com.cn/foms/EN/10.1007/s11706-017-0394-8
https://academic.hep.com.cn/foms/EN/Y2017/V11/I4/307

Fig.1 Scheme 1 Monomer structures used for the preparation of tissue scaffolds.

Fig.2 Scheme 2 Schematic illustration for the fabrication of porous polymer scaffold by the low-temperature solid-state photopolymerization.

Fig.3 SEM images of (a) HEA/PEGDA, (b) HEMA/PEGDA and (c) PEGDA derived polymer scaffolds. (d) Water absorption ratio and porosity percentage of all samples.

Fig.4 The dependency of (a) conversion and (b)polymerization rate at −70°C investigated by using photo-DSC.

Fig.5 SEM images of Ca–P deposition on and inside the surface of (a-1)(a-6) HEA/PEGDA, (b-1)(b-6) HEMA/PEGDA and (c-1)(c-6) PEGDA polymerized scaffolds after the 1st and the 6th mineralization cycles, respectively.

Fig.6 XRD patterns of (a) HEA/PEGDA, (b) HEMA/PEGDA and (c) PEGDA derived scaffolds after 0, the 1st and the 6th mineralization cycles, respectively.

Fig.7 IR peaks of HEA/PEGDA, HEMA/PEGDA and PEGDA derived scaffolds after the 6th mineralization cycle.

Fig.8 TGA curves of (a) HEA/PEGDA, (b) HEMA/PEGDA and (c) PEGDA derived scaffolds before and after mineralization. The insets represent DTG curves.

Fig.9 The MTT test of L929 cells seeded on the scaffolds. *P>0.05 predicted statistically no significant differences when compared to the negative control of indirect cytotoxicity. The data represent mean and standard deviations of six samples.

Fig.10 Fluorescent images of L929 cells seeded on different composite derived scaffolds after the 1st and the 6th mineralization cycles:(a-1)(a-6)HEA/PEGDA; (b-1)(b-6)HEMA/PEGDA; (c-1)(c-6)PEGDA.

1	Nunes-Pereira J, Ribeiro S, Ribeiro C , et al.. Poly (vinylidene fluoride) and copolymers as porous membranes for tissue engineering applications. Polymer Testing, 2015, 44: 234–241 https://doi.org/10.1016/j.polymertesting.2015.05.001
2	Li X M, Cui R R, Sun L W, et al.. 3D-printed biopolymers for tissue engineering application. International Journal of Polymer Science, 2014, 2014: 1–13 https://doi.org/10.1155/2014/829145
3	Chen G, Sato T, Ushida T , et al.. Tissue engineering of cartilage using a hybrid scaffold of synthetic polymer and collagen. Tissue Engineering, 2004, 10(3‒4): 323–330 https://doi.org/10.1089/107632704323061681 pmid: 15165449
4	Kutlusoy T, Oktay B, Apohan N K , et al.. Chitosan-co-hyaluronic acid porous cryogels and their application in tissue engineering. International Journal of Biological Macromolecules, 2017, 103: 366–378 https://doi.org/10.1016/j.ijbiomac.2017.05.067 pmid: 28526348
5	Gomes M E, Reis R L. Tissue engineering: key elements and some trends. Macromolecular Bioscience, 2004, 4(8): 737–742 https://doi.org/10.1002/mabi.200400094 pmid: 15468268
6	Dhandayuthapani B, Yoshida Y, Maekawa T , et al.. Polymeric scaffolds in tissue engineering application: a review. International Journal of Polymer Science, 2011, 609–618 https://doi.org/10.1155/2011/290602
7	Martin I, Obradovic B, Treppo S , et al.. Modulation of the mechanical properties of tissue engineered cartilage. Biorheology, 2000, 37(1‒2): 141–147 pmid: 10912186
8	Bohner M, van Lenthe G H, Grünenfelder S, et al.. Synthesis and characterization of porous β-tricalcium phosphate blocks. Biomaterials, 2005, 26(31): 6099–6105 https://doi.org/10.1016/j.biomaterials.2005.03.026 pmid: 15885772
9	Bose S, Vahabzadeh S, Bandyopadhyay A . Bone tissue engineering using 3D printing. Materials Today, 2013, 16(12): 496–504 https://doi.org/10.1016/j.mattod.2013.11.017
10	Cao H, Kuboyama N. A biodegradable porous composite scaffold of PGA/β-TCP for bone tissue engineering. Bone, 2010, 46(2): 386–395 https://doi.org/10.1016/j.bone.2009.09.031 pmid: 19800045
11	Kim H D, Bae E H, Kwon I C, et al.. Effect of PEG-PLLA diblock copolymer on macroporous PLLA scaffolds by thermally induced phase separation. Biomaterials, 2004, 25(12): 2319–2329 https://doi.org/10.1016/j.biomaterials.2003.09.011 pmid: 14741597
12	Li X, Liu X, Dong W , et al.. In vitro evaluation of porous poly(L-lactic acid) scaffold reinforced by chitin fibers. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2009, 90(2): 503–509 https://doi.org/10.1002/jbm.b.31311 pmid: 19145630
13	Grey C P, Newton S T, Bowlin G L, et al.. Gradient fiber electrospinning of layered scaffolds using controlled transitions in fiber diameter. Biomaterials, 2013, 34(21): 4993–5006 https://doi.org/10.1016/j.biomaterials.2013.03.033 pmid: 23602367
14	Liu H, Nakagawa K, Chaudhary D , et al.. Freeze-dried macroporous foam prepared from chitosan/xanthan gum/montmorillonite nanocomposites. Chemical Engineering Research & Design, 2011, 89(11): 2356–2364 https://doi.org/10.1016/j.cherd.2011.02.023
15	Jain E, Srivastava A, Kumar A . Macroporous interpenetrating cryogel network of poly(acrylonitrile) and gelatin for biomedical applications. Journal of Materials Science: Materials in Medicine, 2009, 20(S1): S173–S179 https://doi.org/10.1007/s10856-008-3504-4 pmid: 18597161
16	Sahiner N, Demirci S. Conducting semi-interpenetrating polymeric composites via the preparation of poly(aniline), poly(thiophene), and poly(pyrrole) polymers within superporous poly(acrylic acid) cryogels. Reactive & Functional Polymers, 2016, 105: 60–65 https://doi.org/10.1016/j.reactfunctpolym.2016.05.017
17	Plieva F M, Karlsson M, Aguilar M R , et al.. Pore structure in supermacroporous polyacrylamide based cryogels. Soft Matter, 2005, 1(4): 303–309 https://doi.org/10.1039/b510010k
18	Liu R, Xu T, Wang C . A review of fabrication strategies and applications of porous ceramics prepared by freeze-casting method. Ceramics International, 2016, 42(2): 2907–2925 https://doi.org/10.1016/j.ceramint.2015.10.148
19	Gutiérrez M C , Ferrer M L , del Monte F . Ice-templated materials: sophisticated structures exhibiting enhanced functionalities obtained after unidirectional freezing and ice-segregation-induced self-assembly. Chemistry of Materials, 2008, 20(3): 634–648 https://doi.org/10.1021/cm702028z
20	Hennink W E, van Nostrum C F. Novel crosslinking methods to design hydrogels. Advanced Drug Delivery Reviews, 2012, 64(Supplement): 223–236 https://doi.org/10.1016/j.addr.2012.09.009
21	Hoffman A S. Hydrogels for biomedical applications. Advanced Drug Delivery Reviews, 2002, 54(1): 3–12 https://doi.org/10.1016/j.addr.2012.09.010 pmid: 11755703
22	Sachlos E, Czernuszka J T. Making tissue engineering scaffolds work. Review: the application of solid freeform fabrication technology to the production of tissue engineering scaffolds. European Cells & Materials, 2003, 5(5): 29–40 https://doi.org/10.22203/eCM.v005a03 pmid: 14562270
23	Lu T, Li Y, Chen T . Techniques for fabrication and construction of three-dimensional scaffolds for tissue engineering. International Journal of Nanomedicine, 2013, 8: 337–350 https://doi.org/10.2147/IJN.S38635 pmid: 23345979
24	Tao Y, Zhang R, Yang W , et al.. Carboxymethylated hyperbranched polysaccharide: Synthesis, solution properties, and fabrication of hydrogel. Carbohydrate Polymers, 2015, 128: 179–187 https://doi.org/10.1016/j.carbpol.2015.04.012 pmid: 26005154
25	Henderson T M , Ladewig K , Haylock D N , et al.. Cryogels for biomedical applications. Journal of Materials Chemistry B: Materials for Biology and Medicine, 2013, 1(21): 2682–2695 https://doi.org/10.1039/c3tb20280a
26	Beauchamp R O , St Clair M B G , Fennell T R , et al.. A critical review of the toxicology of glutaraldehyde. Critical Reviews in Toxicology, 1992, 22(3‒4): 143–174 https://doi.org/10.3109/10408449209145322 pmid: 1388704
27	Plieva F M, Karlsson M, Aguilar M R , et al.. Pore structure of macroporous monolithic cryogels prepared from poly (vinyl alcohol). Journal of Applied Polymer Science, 2006, 100(2): 1057–1066 https://doi.org/10.1002/app.23200
28	Freed L E, Hollander A P, Martin I, et al.. Chondrogenesis in a cell-polymer-bioreactor system. Experimental Cell Research, 1998, 240(1): 58–65 https://doi.org/10.1006/excr.1998.4010 pmid: 9570921
29	Petricoin E F III, Ardekani A M , Hitt B A , et al.. Use of proteomic patterns in serum to identify ovarian cancer. Lancet, 2002, 359(9306): 572–577 https://doi.org/10.1016/S0140-6736(02)07746-2 pmid: 11867112
30	Burdick J A, Anseth K S. Photoencapsulation of osteoblasts in injectable RGD-modified PEG hydrogels for bone tissue engineering. Biomaterials, 2002, 23(22): 4315–4323 https://doi.org/10.1016/S0142-9612(02)00176-X pmid: 12219821
31	Liu Y, Chan-Park M B. Hydrogel based on interpenetrating polymer networks of dextran and gelatin for vascular tissue engineering. Biomaterials, 2009, 30(2): 196–207 https://doi.org/10.1016/j.biomaterials.2008.09.041 pmid: 18922573
32	Hwang Y, Sangaj N, Varghese S . Interconnected macroporous poly(ethylene glycol) cryogels as a cell scaffold for cartilage tissue engineering. Tissue Engineering Part A, 2010, 16(10): 3033–3041 https://doi.org/10.1089/ten.tea.2010.0045 pmid: 20486791
33	Zhu J. Bioactive modification of poly(ethylene glycol) hydrogels for tissue engineering. Biomaterials, 2010, 31(17): 4639–4656 https://doi.org/10.1016/j.biomaterials.2010.02.044 pmid: 20303169
34	Chung B G, Lee K H, Khademhosseini A, et al.. Microfluidic fabrication of microengineered hydrogels and their application in tissue engineering. Lab on a Chip, 2012, 12(1): 45–59 https://doi.org/10.1039/C1LC20859D pmid: 22105780
35	Zhu J, Marchant R E. Design properties of hydrogel tissue-engineering scaffolds. Expert Review of Medical Devices, 2011, 8(5): 607–626 https://doi.org/10.1586/erd.11.27 pmid: 22026626
36	Annabi N, Nichol J W, Zhong X, et al.. Controlling the porosity and microarchitecture of hydrogels for tissue engineering. Tissue Engineering Part B: Reviews, 2010, 16(4): 371–383 https://doi.org/10.1089/ten.teb.2009.0639 pmid: 20121414
37	Van Vlierberghe S , Dubruel P , Schacht E . Biopolymer-based hydrogels as scaffolds for tissue engineering applications: a review. Biomacromolecules, 2011, 12(5): 1387–1408 https://doi.org/10.1021/bm200083n pmid: 21388145
38	Ravichandran R, Venugopal J R, Sundarrajan S, et al.. Precipitation of nanohydroxyapatite on PLLA/PBLG/collagen nanofibrous structures for the differentiation of adipose derived stem cells to osteogenic lineage. Biomaterials, 2012, 33(3): 846–855 https://doi.org/10.1016/j.biomaterials.2011.10.030 pmid: 22048006
39	Omidian H, Park K, Kandalam U , et al.. Swelling and mechanical properties of modified HEMA-based superporous hydrogels. Journal of Bioactive and Compatible Polymers, 2010, 25(5): 483–497 https://doi.org/10.1177/0883911510375175
40	Ji L, Chang W, Cui M , et al.. Photopolymerization kinetics and volume shrinkage of 1, 6-hexanediol diacrylate at different temperature. Journal of Photochemistry and Photobiology A: Chemistry, 2013, 252: 216–221 https://doi.org/10.1016/j.jphotochem.2012.12.010
41	Chang W, Mu X, Zhu X , et al.. Biomimetic composite scaffolds based mineralization of hydroxyapatite on electrospun calcium-containing poly(vinyl alcohol) nanofibers. Materials Science and Engineering C, 2013, 33(7): 4369–4376 https://doi.org/10.1016/j.msec.2013.06.023 pmid: 23910355
42	Rodríguez K , Renneckar S , Gatenholm P . Biomimetic calcium phosphate crystal mineralization on electrospun cellulose-based scaffolds. ACS Applied Materials & Interfaces, 2011, 3(3): 681–689 https://doi.org/10.1021/am100972r pmid: 21355545
43	Li J, Chen Y, Yin Y , et al.. Modulation of nano-hydroxyapatite size via formation on chitosan–gelatin network film in situ. Biomaterials, 2007, 28(5): 781–790 https://doi.org/10.1016/j.biomaterials.2006.09.042 pmid: 17056107
44	Liu M, Dai L, Shi H , et al.. In vitro evaluation of alginate/halloysite nanotube composite scaffolds for tissue engineering. Materials Science and Engineering C, 2015, 49: 700–712 https://doi.org/10.1016/j.msec.2015.01.037 pmid: 25686999
45	Kang Z, Zhang X, Chen Y , et al.. Preparation of polymer/calcium phosphate porous composite as bone tissue scaffolds. Materials Science and Engineering C, 2017, 70(Pt 2): 1125–1131 https://doi.org/10.1016/j.msec.2016.04.008 pmid: 27772713
46	Zhu X, Loh X J. Layer-by-layer assemblies for antibacterial applications. Biomaterials Science, 2015, 3(12): 1505–1518 https://doi.org/10.1039/C5BM00307E pmid: 26415703
47	Dumont V C, Mansur H S, Mansur A A, et al.. Glycol chitosan/nanohydroxyapatite biocomposites for potential bone tissue engineering and regenerative medicine. International Journal of Biological Macromolecules, 2016, 93(Pt B): 1465–1478 https://doi.org/10.1016/j.ijbiomac.2016.04.030 pmid: 27086294
48	Yang D, Zhang J, Xue J , et al.. Electrospinning of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) nanofibers with feature surface microstructure. Journal of Applied Polymer Science, 2013, 127(4): 2867–2874 https://doi.org/10.1002/app.37653
49	Jiang S, Poh Y Z, Loh X J. POSS-based hybrid cationic copolymers with low aggregation potential for efficient gene delivery. RSC Advances, 2015, 5(87): 71322–71328 https://doi.org/10.1039/C5RA12580D
50	Kang Z, Zhang X, Chen Y , et al.. Preparation of polymer/calcium phosphate porous composite as bone tissue scaffolds. Materials Science and Engineering C, 2017, 70(Pt 2): 1125–1131 https://doi.org/10.1016/j.msec.2016.04.008 pmid: 27772713
51	Ma G, Yang D, Wang K , et al.. Organic-soluble chitosan/polyhydroxybutyrate ultrafine fibers as skin regeneration prepared by electrospinning. Journal of Applied Polymer Science, 2010, 118(6): 3619–3624 https://doi.org/10.1002/app.32671
52	Boyan B D, Schwartz Z. Regenerative medicine: Are calcium phosphate ceramics ‘smart’ biomaterials? Nature Reviews Rheumatology, 2011, 7(1): 8–9 https://doi.org/10.1038/nrrheum.2010.210 pmid: 21206482
53	Porter J R, Ruckh T T, Popat K C. Bone tissue engineering: a review in bone biomimetics and drug delivery strategies. Biotechnology Progress, 2009, 25(6): 1539–1560 pmid: 19824042
54	Kretlow J D, Mikos A G. Review: mineralization of synthetic polymer scaffolds for bone tissue engineering. Tissue Engineering, 2007, 13(5): 927–938 https://doi.org/10.1089/ten.2006.0394 pmid: 17430090
55	Shor L, Güçeri S, Wen X , et al.. Fabrication of three-dimensional polycaprolactone/hydroxyapatite tissue scaffolds and osteoblast-scaffold interactions in vitro. Biomaterials, 2007, 28(35): 5291–5297 https://doi.org/10.1016/j.biomaterials.2007.08.018 pmid: 17884162
56	He M, Wang Z, Cao Y , et al.. Construction of chitin/PVA composite hydrogels with jellyfish gel-like structure and their biocompatibility. Biomacromolecules, 2014, 15(9): 3358–3365 https://doi.org/10.1021/bm500827q pmid: 25077674

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