Biomaterials; Bone reconstruction; Protein encapsulation; Silica gel; Sol-gel process; Surface modification
Abstract :
[en] Over the last few years, bone repair has increasingly gained in importance. In recent years, considerable attention has been given to the administration of therapeutic biomolecules to promote tissue regeneration. The aim of this work is the study of the influence of functional groups present at the surface of silica pores and the textural structure on the release kinetics of a model protein (i.e. Soybean Trypsin Inhibitor, STI) and on the preservation of its inhibitory activity. For this purpose, two alternative methods have been investigated: i) impregnation of presynthesized silica gels with the protein solution (i.e. impregnation method), ii) direct incorporation of the protein during the synthesis of the gel (i.e. in situ method). Regarding the impregnation method, a fast release of STI was observed when incubated in physiological conditions (i.e. burst followed by a plateau for the calcined samples or by a sustained release for the dried sample) while the in situ method allowed a better control of the release rate of this protein over the first 24 h. This difference in release kinetics could be explained in terms of the expected geometry of the pores (open versus closed porosity). Interestingly, no significant change in the activity of the protein was noticed for the silica synthesized via the in situ method, while a partial or total loss of inhibitory activity was measured after four weeks of incubation for the impregnated silica.
Disciplines :
Materials science & engineering
Author, co-author :
Tilkin, Rémi ; Université de Liège - ULiège > Department of Chemical Engineering > Nanomaterials, Catalysis, Electrochemistry
Colle, Xavier; Université de Liège - ULiège > Centre Interfacultaire des Biomatériaux (CEIB)
Argento Finol, Anthony; Université de Liège - ULiège > Centre Interfacultaire des Biomatériaux
Regibeau, Nicolas ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Mahy, Julien ; Université de Liège - ULiège > Department of Chemical Engineering > Nanomaterials, Catalysis, Electrochemistry
Grandfils, Christian ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Lambert, Stéphanie ; Université de Liège - ULiège > Department of Chemical Engineering > Nanomaterials, Catalysis, Electrochemistry
Language :
English
Title :
Protein encapsulation in functionalized sol-gel silica: Effect of the encapsulation method on the release kinetics and the activity
Publication date :
08 August 2020
Journal title :
Microporous and Mesoporous Materials
ISSN :
1387-1811
eISSN :
1873-3093
Publisher :
Elsevier, Amsterdam, Netherlands
Volume :
308
Pages :
110502
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Dimitriou, R., Jones, E., McGonagle, D., Giannoudis, P.V., Bone regeneration: current concepts and future directions. BMC Med., 9, 2011, 66, 10.1186/1741-7015-9-66.
Wang, W., Yeung, K.W.K., Bone grafts and biomaterials substitutes for bone defect repair: a review. Bioact. Mater. 2 (2017), 224–247, 10.1016/j.bioactmat.2017.05.007.
Schroeder, J.E., Mosheiff, R., Tissue engineering approaches for bone repair: concepts and evidence. Injury 42 (2011), 609–613, 10.1016/j.injury.2011.03.029.
Brydone, A.S., Meek, D., MacLaine, S., Bone grafting, orthopaedic biomaterials, and the clinical need for bone engineering. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 224 (2010), 1329–1343, 10.1243/09544119JEIM770.
Campana, V., Milano, G., Pagano, E., Barba, M., Cicione, C., Salonna, G., Lattanzi, W., Logroscino, G., Bone substitutes in orthopaedic surgery: from basic science to clinical practice. J. Mater. Sci. Mater. Med. 25 (2014), 2445–2461, 10.1007/s10856-014-5240-2.
US Census Bureau. Statistical Abstracts of the United States: 2012 - Section 1. Population. 2012 accessed www.census.gov/library/publications/2011/compendia/statab/131ed/population.html. (Accessed 25 November 2019)
Santos, E.M., Radin, S., Ducheyne, P., Sol-gel derived carrier for the controlled release of proteins. Biomaterials 20 (1999), 1695–1700, 10.1016/S0142-9612(99)00066-6.
Tilkin, R.G., Mahy, J.G., Régibeau, N., Grandfils, C., Lambert, S.D., Optimization of synthesis parameters for the production of biphasic calcium phosphate ceramics via wet precipitation and sol-gel process. ChemistrySelect 4 (2019), 6634–6641, 10.1002/slct.201901175.
Roy, T.D., Simon, J.L., Ricci, J.L., Rekow, E.D., Thompson, V.P., Parsons, J.R., Performance of degradable composite bone repair products made via three-dimensional fabrication techniques. J. Biomed. Mater. Res. A 66A (2003), 283–291, 10.1002/jbm.a.10582.
Li, X., Liu, X., Wu, S., Yeung, K.W.K., Zheng, Y., Chu, P.K., Design of magnesium alloys with controllable degradation for biomedical implants : from bulk to surface. Acta Biomater. 45 (2016), 2–30, 10.1016/j.actbio.2016.09.005.
Bhattacharyya, S., Wang, H., Ducheyne, P., Polymer-coated mesoporous silica nanoparticles for the controlled release of macromolecules. Acta Biomater. 8 (2012), 3429–3435, 10.1016/j.actbio.2012.06.003.
Lo, K.W., Ulery, B.D., Ashe, K.M., Laurencin, C.T., Studies of bone morphogenetic protein-based surgical repair. Adv. Drug Deliv. Rev. 64 (2012), 1277–1291, 10.1016/j.addr.2012.03.014.
Hwang, C.J., Vaccaro, A.R., Lawrence, J.P., Hong, J., Schellekens, H., Alaoui-Ismaili, M.H., Falb, D., Immunogenicity of bone morphogenetic proteins. J. Neurosurg. Spine SPI 10 (2009), 443–551, 10.3171/2009.1.SPINE08473.
Bessa, P.C., Casal, M., Reis, R.L., Bone morphogenetic proteins in tissue engineering: the road from laboratory to clinic, part II (BMP delivery). J. Tissue Eng. Regen. Med. 2 (2008), 81–96, 10.1002/term.
Kimura, Y., Ph, D., Miyazaki, N., Eng, M., Hayashi, N., Eng, M., Controlled release of bone morphogenetic protein-2 enhances recruitment of osteogenic progenitor cells for de novo generation of bone tissue. Tissue Eng. A 16 (2010), 1263–1270, 10.1089/ten.tea.2009.0322.
Yamashita, J., Furman, B.R., Rawls, H.R., Wang, X., Agrawal, C.M., The use of dynamic mechanical analysis to assess the viscoelastic properties of human cortical bone. J. Biomed. Mater. Res. 58 (2001), 47–53, 10.1002/1097-4636(2001)58:1<47::AID-JBM70>3.0.CO;2-U.
Sun, J., Li, J., Li, C., Yu, Y., Role of bone morphogenetic protein-2 in osteogenic differentiation of mesenchymal stem cells. Mol. Med. Rep. 12 (2015), 4230–4237, 10.3892/mmr.2015.3954.
Zhang, Y., Ma, Y., Yang, M., Min, S., Yao, J., Zhu, L., Expression, purification, and refolding of a recombinant human bone morphogenetic protein 2 in vitro. Protein Expr. Purif. 75 (2011), 155–160, 10.1016/j.pep.2010.07.014.
Jung, H., Yook, S., Han, C., Jang, T., Kim, H., Koh, Y., Estrin, Y., Highly aligned porous Ti scaffold coated with bone morphogenetic protein-loaded silica/chitosan hybrid for enhanced bone regeneration. J. Biomed. Mater. Res. B Appl. Biomater. 102B (2014), 913–921, 10.1002/jbm.b.33072.
Schrier, J.A., Deluca, P.P., Recombinant human bone morphogenetic protein-2 binding and incorporation in PLGA microsphere delivery systems. Pharmaceut. Dev. Technol. 4 (1999), 611–621, 10.1081/PDT-100101400.
Johnson, M.R., Lee, H., Bellamkonda, R.V., Guldberg, R.E., Sustained release of BMP-2 in a lipid-based microtube vehicle. Acta Biomater. 5 (2009), 23–28, 10.1016/j.actbio.2008.09.001.
Li, Y., Song, Y., Ma, A., Li, C., Surface immobilization of TiO2 nanotubes with bone morphogenetic protein-2 synergistically enhances initial preosteoblast adhesion and osseointegration. BioMed Res. Int., 2019, 2019, 5697250, 10.1155/2019/5697250.
Vlasenkova, M.I., Dolinina, E.S., Parfenyuk, E.V., Preparation of mesoporous silica microparticles by sol-gel/emulsion route for protein release. Pharmaceut. Dev. Technol. 24 (2018), 243–252, 10.1080/10837450.2018.1457051.
Yang, W., Hellner, B., Baneyx, F., Self-immobilization of Car9 fusion proteins within high surface area silica sol-gels and dynamic control of protein release. Bioconjugate Chem. 27 (2016), 2450–2459, 10.1021/acs.bioconjchem.6b00406.
Tonon, G., Morpurgo, M., Sol-gel Derived Silica Polymers for the Sustained Release of Proteins. 2008, EP2004727.
Chen, Y.C., Smith, T., Hicks, R.H., Doekhie, A., Koumanov, F., Wells, S.A., Edler, K.J., Van Den Elsen, J., Holman, G.D., Marchbank, K.J., Sartbaeva, A., Thermal stability, storage and release of proteins with tailored fit in silica. Sci. Rep. 7 (2017), 1–8, 10.1038/srep46568.
Chen, Y.-C., Liu, C.-P., Yang, C.-K., Huang, B.-Y., Liu, C.-Y., Preparation and release properties of sol-gel encapsulated proteins. J. Anal. Sci. Methods Instrum. 3 (2013), 11–16, 10.4236/jasmi.2013.33A002.
Zdarta, J., Sałek, K., Kołodziejczak-radzimska, A., Siwińska-stefańska, K., Szwarc-rzepka, K., Norman, M., Klapiszewski, Ł., Bartczak, P., Kaczorek, E., Jesionowski, T., Immobilization of Amano Lipase A onto Stöber silica surface: process characterization and kinetic studies. Open Chem. 13 (2015), 138–148, 10.1515/chem-2015-0017.
Reiner, T., Kababya, S., Gotman, I., Protein incorporation within Ti scaffold for bone ingrowth using Sol-gel SiO2 as a slow release carrier. J. Mater. Sci. Mater. Med. 19 (2008), 583–589, 10.1007/s10856-007-3194-3.
Ronda, L., Bruno, S., Campanini, B., Mozzarelli, A., Abbruzzetti, S., Immobilization of proteins in silica gel: biochemical and biophysical properties. Curr. Org. Chem. 19 (2015), 15–18, 10.2174/1385272819666150601211349.
Brinker, C.J., Scherer, G.W., Sol-Gel Science: the Physics and Chemistry of Sol-Gel Processing. 1990, Academic Press, San Diego, CA, 10.1016/B978-0-08-057103-4.50006-4.
Lambert, S., Alié, C., Pirard, J.P., Heinrichs, B., Study of textural properties and nucleation phenomenon in Pd/SiO2, Ag/SiO2 and Cu/SiO2 cogelled xerogel catalysts. J. Non-Cryst. Solids 342 (2004), 70–81, 10.1016/j.jnoncrysol.2004.06.005.
Andreani, T., de Souza, A.L.R., Silva, A.M., Souto, E.B., Sol–gel carrier system: a novel controlled Drug delivery. Souto, E.B., (eds.) Patenting Nanomedicines Leg. Asp. Intellect. Prop. Grant Oppor., 2012, Springer-Verlag Berlin Heidelberg, Heidelberg, 1551–1660, 10.1007/978-3-642-29265-1.
Wang, X., Ben Ahmed, N., Alvarez, G.S., V Tuttolomondo, M., Hélary, C., Desimone, M.F., Coradin, T., Sol-gel encapsulation of biomolecules and cells for medicinal applications. Curr. Top. Med. Chem. 15 (2015), 223–244, 10.2174/1568026614666141229112734.
Jin, W., Brennan, J.D., Properties and applications of proteins encapsulated within sol-gel derived materials. Anal. Chim. Acta 461 (2002), 1–36, 10.1016/S0003-2670(02)00229-5.
Anderson, A.M., Carroll, M.K., Green, E.C., Melville, J.T., Bono, M.S., Hydrophobic silica aerogels prepared via rapid supercritical extraction. J. Sol. Gel Sci. Technol. 53 (2010), 199–207, 10.1007/s10971-009-2078-z.
Shao, Z., Cheng, X., Zheng, Y., Facile co-precursor sol-gel synthesis of a novel amine-modified silica aerogel for high efficiency carbon dioxide capture. J. Colloid Interface Sci. 530 (2018), 412–423, 10.1016/j.jcis.2018.06.094.
He, Q., Shi, J., Zhu, M., Chen, Y., Chen, F., The three-stage in vitro degradation behavior of mesoporous silica in simulated body fluid. Microporous Mesoporous Mater. 131 (2010), 314–320, 10.1016/j.micromeso.2010.01.009.
Livage, J., Coradin, T., Roux, C., Encapsulation of biomolecules in silica gels. J. Phys. Condens. Matter 13 (2001), R673–R691, 10.1088/0953-8984/13/33/202.
Hum, J., Boccaccini, A.R., Bioactive glasses as carriers for bioactive molecules and therapeutic drugs : a review. J. Mater. Sci. Mater. Med. 23 (2012), 2317–2333, 10.1007/s10856-012-4580-z.
Agrawal, C.M., Best, J., Heckman, J.D., Boyan, B.D., Protein release kinetics of a biodegradable implant for fracture. Biomaterials 16 (1995), 1255–1260, 10.1016/0142-9612(95)98133-Y.
Chaudhari, A., Mv, C., Martens, J., Vandamme, K., Naert, I., Bone, D.J., Bone tissue response to BMP-2 adsorbed on amorphous microporous silica implants. J. Clin. Periodontol. 39 (2012), 1206–1213, 10.1111/jcpe.12005.
Chaudhari, A., Duyck, J., Braem, A., Vleugels, J., Logeart-avramoglou, H.P.D., Naert, I., Martens, J.A., Vandamme, K., Modified titanium surface-mediated effects on human bone marrow stromal cell response. Materials (Basel) 2 (2013), 5533–5548, 10.3390/ma6125533.
Tang, W., Lin, D., Yu, Y., Niu, H., Guo, H., Yuan, Y., Liu, C., Bioinspired trimodal macro/micro/nano-porous scaffolds loading rhBMP-2 for complete regeneration of critical size bone defect. Acta Biomater. 32 (2016), 309–323, 10.1016/j.actbio.2015.12.006.
Li, X., Lin, W., Xing, F., The degradation and BMP release dynamics of silica-based xerogels modified by adding calcium and magnesium or sintering process. Appl. Mech. Mater. 151 (2012), 378–382, 10.4028/www.scientific.net/AMM.151.378.
Nicoll, S.B., Radin, S., Santos, E.M., Tuan, R.S., Ducheyne, P., In vitro release kinetics of biologically active transforming growth factor-β1 from a novel porous glass carrier. Biomaterials 18 (1997), 853–859, 10.1016/S0142-9612(97)00008-2.
Mahy, J.G., Tasseroul, L., Zubiaur, A., Geens, J., Brisbois, M., Herlitschke, M., Hermann, R., Heinrichs, B., Lambert, S.D., Highly dispersed iron xerogel catalysts for p-nitrophenol degradation by photo-Fenton effects. Microporous Mesoporous Mater. 197 (2014), 164–173, 10.1016/j.micromeso.2014.06.009.
Lecloux, A., Exploitation des isothermes d'adsorption et de désorption d'azote pour l’étude de la texture des solides poreux. Mém. Soc. Des Sci. Liege 4 (1971), 169–209.
Lecloux, A., Texture of catalysts. Anderson, J.R., Boudart, M., (eds.) Catal. Sci. Technol., vol. 2, 1981, Springer, Berlin, 171, 10.1007/978-3-642-93247-2.
Pirard, R., Heinrichs, B., Cantfort, O.V.A.N., Pirard, J.P., Mercury porosimetry applied to low density Xerogels; relation between structure and mechanical properties. J. Sol. Gel Sci. Technol. 13 (1998), 335–339, 10.1023/A:1008676211157.
Park, J., Regalbuto, J.R., A simple, accurate determination of oxide PZC and the strong buffering effect of oxide surfaces at incipient wetness. J. Colloid Interface Sci. 175 (1995), 239–252, 10.1006/jcis.1995.1452.
Lambert, S., Job, N., Souza, L.D., Fernando, M., Pereira, R., Pirard, R., Heinrichs, B., Luis, J., Pirard, J., Regalbuto, J.R., Synthesis of very highly dispersed platinum catalysts supported on carbon xerogels by the strong electrostatic adsorption method. J. Catal. 261 (2009), 23–33, 10.1016/j.jcat.2008.10.014.
Lowry, O.H., Rosebrough, N.J., Farr, L.A., Randall, R.J., Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951), 265–275, 10.1016/0304-3894(92)87011-4.
Merck, Enzymatic Assay of Trypsin Inhibitor. 2020 accessed https://www.sigmaaldrich.com/technical-documents/protocols/biology/enzymatic-assay-of-trypsin-inhibitor.html. (Accessed 27 April 2018)
Mansur, H., Oréfice, R., Pereira, M., Lobato, Z., FTIR and UV-vis study of chemically engineered biomaterial surfaces for protein immobilization. Spectroscopy 16 (2002), 351–360, 10.1155/2002/183053.
Péré, E., Cardy, H., Cairon, O., Simon, M., Lacombe, S., Quantitative assessment of organic compounds adsorbed on silica gel by FTIR and UV-VIS spectroscopies: the contribution of diffuse reflectance spectroscopy. Vib. Spectrosc. 25 (2001), 163–175, 10.1016/S0924-2031(00)00113-2.
Antony, R., Theodore David Manickam, S., Kollu, P., Chandrasekar, P.V., Karruppasamy, K., Balakumar, S., Highly dispersed Cu(II), Co(II) and Ni(II) catalysts covalently immobilized on imine-modified silica for cyclohexane oxidation with hydrogen peroxide. RSC Adv. 4 (2014), 24820–24830, 10.1039/C4RA01960A.
Capeletti, L.B., Baibich, I.M., Butler, I.S., dos Santos, J.H.Z., Infrared and Raman spectroscopic characterization of some organic substituted hybrid silicas. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 133 (2014), 619–625, 10.1016/j.saa.2014.05.072.
Osswald, J., Fehr, K.T., FTIR spectroscopic study on liquid silica solutions and nanoscale particle size determination. J. Mater. Sci. 41 (2006), 1335–1339, 10.1007/s10853-006-7327-8.
Warring, S.L., Beattie, D.A., Mcquillan, A.J., Sur fi cial siloxane-to-silanol interconversion during room- temperature hydration/dehydration of amorphous silica films observed by ATR-IR and TIR-Raman spectroscopy. Langmuir 32 (2016), 1568–1576, 10.1021/acs.langmuir.5b04506.
Etienne, M., Walcarius, A., Analytical investigation of the chemical reactivity and stability of aminopropyl-grafted silica in aqueous medium. Talanta 59 (2003), 1173–1188, 10.1016/S0039-9140(03)00024-9.
Adumeau, L., Genevois, C., Roudier, L., Schatz, C., Adumeau, L., Genevois, C., Roudier, L., Schatz, C., Couillaud, F., Impact of surface grafting density of PEG macromolecules on dually fluorescent silica nanoparticles used for the in vivo imaging of subcutaneous tumors. Biochim. Biophys. Acta 1861 (2017), 1587–1596, 10.1016/j.bbagen.2017.01.036.
Bharathi, S., Fishelson, N., Lev, O., Direct synthesis and characterization of gold and other noble metal nanodispersions in sol - gel-derived organically modified silicates. Langmuir 15 (1999), 1929–1937, 10.1021/la980490x.
Zhuravlev, L.T., Concentration of hydroxyl groups on the surface of amorphous silicas. Langmuir 3 (1987), 316–318, 10.1021/la00075a004.
Belton, D.J., Deschaume, O., Perry, C.C., An overview of the fundamentals of the chemistry of silica with relevance to biosilicification and technological advances. FEBS J. 279 (2012), 1710–1720, 10.1111/j.1742-4658.2012.08531.x.An.
Thommes, M., Kaneko, K., V Neimark, A., Olivier, J.P., Rodriguez-reinoso, F., Rouquerol, J., Sing, K.S.W., Physisorption of gases, with special reference to the evaluation of surface area and pore size distribution (IUPAC Technical Report). Pure Appl. Chem. 87 (2015), 1051–1069, 10.1515/pac-2014-1117.
Alié, C., Ferauche, F., Pirard, R., Lecloux, A.J., Pirard, J.-P., Preparation of low-density xerogels by incorporation of additives during synthesis. J. Non-Cryst. Solids 289 (2001), 88–96, 10.1016/S0022-3093(01)00697-4.
Kosmulski, M., Compilation of PZC and IEP of sparingly soluble metal oxides and hydroxides from literature. Adv. Colloid Interface Sci. 152 (2009), 14–25, 10.1016/j.cis.2009.08.003.
Cassano, D., Mapanao, A.-K., Summa, M., Vlamidis, Y., Giannone, G., Santi, M., Guzzolino, E., Pitto, L., Poliseno, L., Bertorelli, R., Voliani, V., Biosafety and biokinetics of noble metals: the impact of their chemical nature. ACS Appl. Biomater. 2 (2019), 4464–4470, 10.1021/acsabm.9b00630.
Yildirim, A., Ozgur, E., Bayindir, M., Impact of mesoporous silica nanoparticle surface functionality on hemolytic activity, thrombogenicity and non-specific protein adsorption. J. Mater. Chem. B. 1 (2013), 1909–1920, 10.1039/c3tb20139b.
Schlipf, D.M., Rankin, S.E., Knutson, B.L., Pore-size dependent protein adsorption and protection from proteolytic hydrolysis in tailored mesoporous silica particles. ACS Appl. Mater. Interfaces 5 (2013), 10111–10117, 10.1021/am402754h.
Song, H.K., Suh, S.W., Kunitz-type soybean trypsin inhibitor Revisited : refined structure of its complex with porcine trypsin reveals an insight into the interaction between a homologous inhibitor from Erythrina caffra and tissue-type plasminogen activator. J. Mol. Biol. 275 (1998), 347–363, 10.1006/jmbi.1997.1469.
Thorat, A.A., Suryanarayanan, R., Characterization of phosphate buffered saline (PBS) in frozen state and after freeze-drying. Pharm. Res. (N. Y.), 36, 2019, 98, 10.1007/s11095-019-2619-2.
Scheufler, C., Sebald, W., Hülsmeyer, M., Crystal structure of human bone morphogenetic protein-2 at 2.7 Å resolution1. J. Mol. Biol. 287 (1999), 103–115, 10.1006/jmbi.1999.2590.
Chang, Y., Liu, T.C., Tsai, M., Selective isolation of trypsin inhibitor and lectin from soybean whey by chitosan/tripolyphosphate/genipin Co-crosslinked beads. Int. J. Mol. Sci. 15 (2014), 9979–9990, 10.3390/ijms15069979.
Yang, J., Shi, P., Tu, M., Wang, Y., Liu, M., Fan, F., Du, M., Bone morphogenetic proteins: relationship between molecular structure and their osteogenic activity. Food Sci. Hum. Wellness 3 (2014), 127–135, 10.1016/j.fshw.2014.12.002.
