Pectin has recently attracted increasing attention for biomedical and pharmaceutical applications. Due to the lack of adhesion molecules in polysaccharides, phenolic hydroxyl conjugated gelatin was added to enzymatically-gellable peroxidase-modified pectin derivative and compared with phenolic hydroxyl -pectin/collagen. Both pectin and gelatin were modified by tyramine hydrochloride in the presence of EDC/NHS. The phenolic hydroxyl -pectin/phenolic hydroxyl -gelatin, phenolic hydroxyl-pectin/collagen, and phenolic hydroxyl -pectin hydrogels were prepared using horseradish peroxidase and hydrogen peroxide. The hydrogels were characterized by gelation time analysis. Morphology, enzymatic biodegradation, mechanical and swelling properties as well as water vapor transmission rate were also evaluated. Fibroblasts were cultured for 7 days, and the survival rate was evaluated using conventional MTT assay. Hydrogels composed of Ph-pectin/Ph-gelatin showed decreased biodegradation rate, and WVTR and further improved mechanical performance in comparison with other groups. Both phenolic hydroxyl -pectin/collagen and phenolic hydroxyl -pectin/phenolic hydroxyl -gelatin hydrogels exhibited porous structures. The hydrogels composed of collagen promoted cell survival rate 1.4 and 3.5 times compared to phenolic hydroxyl -gelatin and phenolic hydroxyl -pectin based hydrogels at the end of 7 days, respectively (p < 0.001). The study demonstrated the potential of enzymatically-gellable pectin-based hydrogels as cost-effective frameworks for use in tissue engineering applications.
ChenF-MLiuX.Advancing biomaterials of human origin for tissue engineering. 2016;
53: 86–168.
2.
ChanBLeongK.Scaffolding in tissue engineering: general approaches and tissue-specific considerations. 2008;
17: 467–79.
3.
GylesDACastroLDSilvaJOCJr, et al.
A review of the designs and prominent biomedical advances of natural and synthetic hydrogel formulations. 2017;
88: 373–92.
4.
RanganathanNJoseph BensinghRAbdul KaderM, et al.
Synthesis and Properties of Hydrogels Prepared by Various Polymerization Reaction Systems. 2018; 1–25.
5.
Morshedloo F, Khoshfetrat AB, Kazemi D, et al. Gelatin improves peroxidase-mediated alginate hydrogel characteristics as a potential injectable hydrogel for soft tissue engineering applications. J Biomed Mater Res B 2020; 108: 2950-60.
6.
SpicerCD.Hydrogel scaffolds for tissue engineering: the importance of polymer choice. Polym Chem2020;
11: 184–219.
7.
NevesSCGomesDBSousaA, et al.
Biofunctionalized pectin hydrogels as 3D cellular microenvironments. 2015;
3: 2096–108.
8.
Lara-EspinozaCCarvajal-MillanEBalandran-QuintanaR, et al.
Pectin and pectin-based composite materials: beyond food texture. Molecules2018;
23: 942.
9.
KeJJiangGShenG, et al.
Optimization, characterization and rheological behavior study of pectin extracted from chayote (sechium edule) using ultrasound assisted method. Int J Biol Macromol2020;
147: 688–698.
10.
MongkolkitikulSParadeeNSirivatA.Electrically controlled release of ibuprofen from conductive poly (3-methoxydiphenylamine)/crosslinked pectin hydrogel. Eur J Pharm Sci2018;
112: 20–27.
11.
TakeiTSugiharaKIjimaH, et al.
In situ gellable sugar beet pectin via enzyme-catalyzed coupling reaction of feruloyl groups for biomedical applications. J Biosci Bioeng2011;
112: 491–494.
12.
RoseJBPacelliSHajAJE, et al.
Gelatin-based materials in ocular tissue engineering. Materials (Basel)2014;
7: 3106–3135.
13.
TabataYIkadaY.Protein release from gelatin matrices. Adv Drug Deliv Rev1998;
31: 287–301.
14.
MishraRMajeedABanthiaA.Development and characterization of pectin/gelatin hydrogel membranes for wound dressing. Int J Plast Technol2011;
15: 82–95.
15.
DangXLiYYangM.Biodegradable waterborne polyurethane grafted with gelatin hydrolysate via solvent-free copolymerization for potential porous scaffold material. J Mech Behav Biomed Mater2019;
92: 79–89.
16.
BodeFDa SilvaMADrakeAF, et al.
Enzymatically cross-linked tilapia gelatin hydrogels: physical, chemical, and hybrid networks. Biomacromolecules2011;
12: 3741–3752.
17.
DashRFostonMRagauskasAJ.Improving the mechanical and thermal properties of gelatin hydrogels cross-linked by cellulose nanowhiskers. Carbohydr Polym2013;
91: 638–645.
18.
GoldTBBuiceRGLodderRA, et al.
Determination of extent of formaldehyde-induced crosslinking in hard gelatin capsules by near-infrared spectrophotometry. Pharm Res1997;
14: 1046–1050.
19.
LiuWGDe YaoKWangGC, et al.
Intrinsic fluorescence investigation on the change in conformation of cross-linked gelatin gel during volume phase transition. Polymer2000;
41: 7589–7592.
20.
HanBHuangLCheungD, et al.
Polypeptide growth factors with a collagen binding domain: Their potential for tissue repair and organ regeneration. Tissue Engineering of Vascular Prosthetic Grafts Austin: RG Landes1999; 287–299.
21.
KhatamiNKhoshfetratABKhaksarM, et al.
Collagen‐alginate‐nano‐silica microspheres improved the osteogenic potential of human osteoblast‐like MG‐63 cells. J Cell Biochem2019;
120: 15069–15082.
22.
MirzaeiE.Evaluating the effect of pH on mechanical strength and cell compatibility of nanostructured collagen hydrogel by the plastic compression method. Nanomed J2018;
5: 180–185.
23.
TranquilloRT. Self-organization of tissue-equivalents: the nature and role of contact guidance. Biochem Soc Symp 1999; 65: 27–42.
24.
SakaiSHiroseKTaguchiK, et al.
An injectable, in situ enzymatically gellable, gelatin derivative for drug delivery and tissue engineering. Biomaterials2009;
30: 3371–3377.
25.
Hoang ThiTTLeeYRyuSB, et al.
Enhanced tissue adhesiveness of injectable gelatin hydrogels through dual catalytic activity of horseradish peroxidase. Biopolymers2018;
109: e23077.
26.
TranNQJoungYKLihE, et al.
Supramolecular hydrogels exhibiting fast in situ gel forming and adjustable degradation properties. Biomacromolecules2010;
11: 617–625.
27.
FirouziNBaradar KhoshfetratAKazemiD.Enzymatically gellable gelatin improves nano‐hydroxyapatite‐alginate microcapsule characteristics for modular bone tissue formation. J Biomed Mater Res A2020;
108: 340–350.
28.
AlizadehMAbbasiFKhoshfetratA, et al.
Microstructure and characteristic properties of gelatin/chitosan scaffold prepared by a combined freeze-drying/leaching method. 2013;
33: 3958–67.
29.
XuQGuoLSigenA, et al.
Injectable hyperbranched poly (β-amino ester) hydrogels with on-demand degradation profiles to match wound healing processes. Chem Sci2018;
9: 2179–2187.
30.
LianSXiaoYBianQ, et al.
Injectable hydrogel as stem cell scaffolds from the thermosensitive terpolymer of NIPAAm/AAc/HEMAPCL. Int J Nanomedicine2012;
7: 4893–4905.
31.
MousaviSKhoshfetratABKhatamiN, et al.
Comparative study of collagen and gelatin in chitosan-based hydrogels for effective wound dressing: Physical properties and fibroblastic cell behavior. Biochemical and Biophysical Research Communications2019;
518: 625–631.
32.
Veitch NC. Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry 2004; 65: 249–259.
LeeYBaeJWOhDH, et al.
In situ forming gelatin-based tissue adhesives and their phenolic content-driven properties. J Mater Chem B2013;
1: 2407–2414.
35.
MatheisGWhitakerJR.Peroxidase-catalyzed cross linking of proteins. J Protein Chem1984;
3: 35–48.
36.
WenpoFGaofengLShuyingF, et al.
Preparation and characterization of collagen–hydroxyapatite/pectin composite. Int J Biol Macromol2015;
74: 218–223.
37.
JinRLinCCaoA.Enzyme-mediated fast injectable hydrogels based on chitosan–glycolic acid/tyrosine: preparation, characterization, and chondrocyte culture. Polymer Chemistry2014;
5: 391–398.
38.
HendersonTMLadewigKHaylockDN, et al.
Cryogels for biomedical applications. J Mater Chem B2013;
1: 2682–2695.
39.
AlizadehMAbbasiFKhoshfetratA, et al.
Microstructure and characteristic properties of gelatin/chitosan scaffold prepared by a combined freeze-drying/leaching method. Mater Sci Eng C Mater Biol Appl2013;
33: 3958–3967.
40.
GorthDWebsterT.Matrices for tissue engineering and regenerative medicine. Biomaterials for artificial organs.
Amsterdam:
Elsevier, 2011, pp. 270–286.
41.
MerinoSMartinCKostarelosK, et al.
Nanocomposite hydrogels: 3D polymer–nanoparticle synergies for on-demand drug delivery. ACS Nano2015;
9: 4686–4697.
42.
NaeemFKhanSJalilA, et al.
pH responsive cross-linked polymeric matrices based on natural polymers: effect of process variables on swelling characterization and drug delivery properties. Bioimpacts2017;
7: 177–192.
43.
FukuokaTUyamaHKakuchiT, et al.
Synthesis of a new class of high‐molecular‐weight soluble poly (amino acid) s by oxidative polymerization of polyfunctional macromolecules. Macromol Rapid Commun2002;
23: 698–702.
44.
ChuangC-HLinR-ZMelero-MartinJM, et al.
Comparison of covalently and physically cross-linked collagen hydrogels on mediating vascular network formation for engineering adipose tissue. Artif Cells Nanomed Biotechnol2018;
46: S434–S447.
45.
ProkopijevicMProdanovicOSpasojevicD, et al.
Tyramine-modified pectins via periodate oxidation for soybean hull peroxidase induced hydrogel formation and immobilization. Appl Microbiol Biotechnol2017;
101: 2281–2290.
46.
AkhgariAFarahmandFGarekaniHA, et al.
The effect of pectin on swelling and permeability characteristics of free films containing eudragit RL and/or RS as a coating formulation aimed for colonic drug delivery. Daru2010;
18: 91–96.
47.
VedadghavamiAMinooeiFMohammadiMH, et al.
Manufacturing of hydrogel biomaterials with controlled mechanical properties for tissue engineering applications. Acta Biomater2017;
62: 42–63.
48.
FarrisSSchaichKMLiuL, et al.
Gelatin–pectin composite films from polyion-complex hydrogels. Food Hydrocolloids2011;
25: 61–70.
49.
OudgenoegGHilhorstRPiersmaSR, et al.
Peroxidase-mediated cross-linking of a tyrosine-containing peptide with ferulic acid. J Agric Food Chem2001;
49: 2503–2510.
50.
TavakolMVasheghani-FarahaniESoleimaniM, et al.
Synthesis and characterization of an enzyme mediated in situ forming hydrogel based on gum tragacanth for biomedical applications. Iran J Biotech2014;
12: 42–49.
51.
KhanmohammadiMDastjerdiMBAiA, et al.
Horseradish peroxidase-catalyzed hydrogelation for biomedical applications. Biomater Sci2018;
6: 1286–1298.
52.
ZahediPRezaeianIRanaei‐SiadatSO, et al.
A review on wound dressings with an emphasis on electrospun nanofibrous polymeric bandages. Polym Adv Technol2010;
21: 77–95.
53.
DiasABragaMSeabraI, et al.
Development of natural-based wound dressings impregnated with bioactive compounds and using supercritical carbon dioxide. Int J Pharm2011;
408: 9–19.
54.
LeeKYMooneyDJ.Hydrogels for tissue engineering. Chem Rev2001;
101: 1869–1880.
55.
MauriESacchettiAVicarioN, et al.
Evaluation of RGD functionalization in hybrid hydrogels as 3D neural stem cell culture systems. Biomater Sci2018;
6: 501–510.
56.
BuckleyCTO'KellyKU.Maintaining cell depth viability: on the efficacy of a trimodal scaffold pore architecture and dynamic rotational culturing. J Mater Sci Mater Med2010;
21: 1731–1738.
57.
RekhaKRSelvakumarGP.Gene expression regulation of Bcl2, bax and cytochrome-C by geraniol on chronic MPTP/probenecid induced C57BL/6 mice model of Parkinson’s disease. Chem Biol Interact2014;
217: 57–66.
58.
JungYJLeeASNguyen-ThanhT, et al.
SIRT2 regulates LPS-induced renal tubular CXCL2 and CCL2 expression. J Am Soc Nephrol2015;
26: 1549–1560.
59.
HenningssonLEneljungTJirholtP, et al.
Disease-dependent local IL-10 production ameliorates collagen induced arthritis in mice. PLoS One2012;
7: e49731.
60.
KhaksarMSayyariMRezaieJ, et al.
High glucose condition limited the angiogenic/cardiogenic capacity of murine cardiac progenitor cells in in vitro and in vivo milieu. Cell Biochem Funct2018;
36: 346–356.
