Cellulose nano-dispersions enhanced by ultrasound assisted chemical modification drive osteoblast proliferation and differentiation in PVA/HA bone tissue engineering scaffolds.
Zhu, Shunshun; Sun, Hongnan; Mu, Taihuaet al.
2024 • In International Journal of Biological Macromolecules, 279 (Pt 4), p. 135571
[en] To develop a biological bone tissue scaffold with uniform pore size and good cell adhesion was both challenging and imperative. We prepared modified cellulose nanocrystals (CNCs) dispersants (K-PCNCs) by ultrasound-assisted alkylation modification. Subsequently, nano-hydroxyapatite (HC-K) was synthesized using K-PCNCs as a dispersant and composited with polyvinyl alcohol (PVA) to prepare the scaffold using the ice template method. The results showed that the water contact angle and degree of substitution (135°, 1.53) of the K-PCNCs were highest when the ultrasound power was 450 W and the time was 2 h. The dispersion of K-PCNCs prepared under this condition was optimal. SEM showed that the pore distribution of the composite scaffolds was more homogeneous than the PVA scaffold. The porosity, equilibrium swelling rate, and mechanical properties of the composite scaffolds increased and then decreased with the increase of HC-K content, and reached the maximum values (56.1 %, 807.7 %, and 0.085 ± 0.004 MPa) at 9 % (w/w) of HC-K content. Cell experiments confirmed scaffold has good cytocompatibility and mineralization capacity. The ALP activity reached 1.71 ± 0.25 (ALP activity/mg protein). In conclusion, the scaffolds we developed have good biocompatibility and mechanical properties and have great potential in promoting bone defect repair.
Disciplines :
Chemistry
Author, co-author :
Zhu, Shunshun ; Université de Liège - ULiège > TERRA Research Centre ; Laboratory of Food Chemistry and Nutrition Science, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, No. 2 Yuan Ming Yuan West Road, Haidian District, P.O. Box 5109, Beijing 100193, China
Sun, Hongnan; Laboratory of Food Chemistry and Nutrition Science, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, No. 2 Yuan Ming Yuan West Road, Haidian District, P.O. Box 5109, Beijing 100193, China. Electronic address: sunhongnan@caas.cn
Mu, Taihua; Laboratory of Food Chemistry and Nutrition Science, Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences, Key Laboratory of Agro-Products Processing, Ministry of Agriculture and Rural Affairs, No. 2 Yuan Ming Yuan West Road, Haidian District, P.O. Box 5109, Beijing 100193, China. Electronic address: mutaihua@126.com
Richel, Aurore ; Université de Liège - ULiège > Département GxABT > Chemistry for Sustainable Food and Environmental Systems (CSFES)
Language :
English
Title :
Cellulose nano-dispersions enhanced by ultrasound assisted chemical modification drive osteoblast proliferation and differentiation in PVA/HA bone tissue engineering scaffolds.
Publication date :
12 September 2024
Journal title :
International Journal of Biological Macromolecules
ISSN :
0141-8130
eISSN :
1879-0003
Publisher :
Elsevier B.V., Netherlands
Volume :
279
Issue :
Pt 4
Pages :
135571
Peer reviewed :
Peer Reviewed verified by ORBi
Development Goals :
3. Good health and well-being 12. Responsible consumption and production
The authors gratefully acknowledge the earmarked fund for CARS (CARS-10) , and the Science and Technology Innovation Project of the Chinese Academy of Agricultural Sciences ( CAAS-ASTIP-202X-IFST ).
Roman, M., Haring, A.P., Bertucio, T.J., The growing merits and dwindling limitations of bacterial cellulose-based tissue engineering scaffolds. Curr. Opin. Chem. Eng., 24, 2019, 10.1016/j.coche.2019.03.006.
Feng, P., Zhao, R., Tang, W., Yang, F., Tian, H., Peng, S., Pan, H., Shuai, C., Structural and functional adaptive artificial bone: materials, fabrications, and properties. Adv. Funct. Mater., 33, 2023, 10.1002/adfm.202214726.
Rahmani Del Bakhshayesh, A., Babaie, S., Tayefi Nasrabadi, H., Asadi, N., Akbarzadeh, A., Abedelahi, A., An overview of various treatment strategies, especially tissue engineering for damaged articular cartilage. Artif. Cells Nanomed. Biotechnol., 48, 2020, 10.1080/21691401.2020.1809439.
Kumar, A., Negi, Y.S., Choudhary, V., Bhardwaj, N.K., Microstructural and mechani- cal properties of porous biocomposite scaffolds based on polyvinyl alcohol, nano-hydroxyapatite and cellulose nanocrystals. Cellulose, 21, 2014, 10.1007/s10570-014-0339-7.
Ashraf, A.A., Zebarjad, S.M., Hadianfard, M.J., The cross-linked polyvinyl alcohol/ hydroxyapatite nanocomposite foam. J. Mater. Res. Technol., 8, 2019, 10.1016/j.jmrt.2019.02.024.
Yu, L., Rowe, D.W., Perera, I.P., Zhang, J., Suib, S.L., Xin, X., Wei, M., Intrafibrillar mineralized collagen-hydroxyapatite-based scaffolds for bone regeneration. ACS Appl. Mater. Interfaces, 12, 2020, 10.1021/acsami.0c00275.
de Santis, R., Russo, A., Gloria, A., D'Amora, U., Russo, T., Panseri, S., Sandri, M., Tampieri, A., Marcacci, M., Dediu, V.A., Wilde, C.J., Ambrosio, L., Towards the design of 3D fiber-deposited poly(ε-caprolactone)/iron-doped hydroxyapatite nanocomposite magnetic scaffolds for bone regeneration. J. Biomed. Nanotechnol., 11, 2015, 10.1166/jbn.2015.2065.
Irfa'i, M.A., Schmahl, W.W., Pusparizkita, Y.M., Muryanto, S., Prihanto, A., Ismail, R., Jamari, J., Bayuseno, A.P., Hydrothermally synthesized-nanoscale carbonated hydroxyapatite with calcium carbonates derived from green mussel shell wastes. J. Mol. Struct., 1306, 2024, 10.1016/j.molstruc.2024.137837.
Peng, S.Y., Lin, Y.W., Lin, Y.Y., Lin, K.L., Hydrothermal synthesis of hydroxyapatite nanocrystals from calcium-rich limestone sludge waste: preparation, characteri- zation, and application for Pb2+ adsorption in aqueous solution. Inorg. Chem. Commun., 160, 2024, 10.1016/j.inoche.2023.111943.
Lee, K., Kwon, K.Y., Preparation of amine-incorporated hydroxyapatite through a single-step hydrothermal reaction. Mater. Lett., 355, 2024, 10.1016/j.matlet.2023.135508.
Pang, S., An, H., Zhao, X., Wang, Y., Ionic liquid-assisted preparation of hydroxy- apatite and its catalytic performance for decarboxylation of itaconic acid. Chin. J. Chem. Eng., 67, 2024, 10.1016/j.cjche.2023.11.018.
Abdian, N., Etminanfar, M., Sheykholeslami, S.O.R., Hamishehkar, H., Khalil-Allafi, J., Preparation and characterization of chitosan/hydroxyapatite scaffolds containing mesoporous SiO2-HA for drug delivery applications. Mater. Chem. Phys., 301, 2023, 10.1016/j.matchemphys.2023.127672.
Wan, L., Cui, B., Wang, L., A review on preparation raw materials, synthesis methods, and modifications of hydroxyapatite as well as their environmental applications. Sustain. Chem. Pharm., 38, 2024, 10.1016/j.scp.2024.101447.
Sebastiammal, S., Fathima, A.S.L., Al-Ghanim, K.A., Nicoletti, M., Baskar, G., Iyyappan, J., Govindarajan, M., Synthesis and characterization of magnesium-wrapped hydroxyapatite nanomaterials for biomedical applications. Surf. Interfaces, 44, 2024, 10.1016/j.surfin.2023.103779.
Zainal, S.H., Mohd, N.H., Suhaili, N., Anuar, F.H., Lazim, A.M., Othaman, R., Preparation of cellulose-based hydrogel: a review. J. Mater. Res. Technol., 10, 2021, 10.1016/j.jmrt.2020.12.012.
Seddiqi, H., Oliaei, E., Honarkar, H., Jin, J., Geonzon, L.C., Bacabac, R.G., Klein-Nulend, J., Cellulose and its derivatives: towards biomedical applications. Cellulose 28 (2021), 1893–1931, 10.1007/s10570-020-03674-w.
Panyasiri, P., Lam, N.T., Sukyai, P., The effect of hydroxyapatite prepared by in situ synthesis on the properties of poly(vinyl alcohol)/cellulose nanocrystals biomaterial. J. Polym. Environ., 28, 2020, 10.1007/s10924-019-01599-5.
Grishkewich, N., Mohammed, N., Tang, J., Tam, K.C., Recent advances in the application of cellulose nanocrystals. Curr. Opin. Colloid Interface Sci., 29, 2017, 10.1016/j.cocis.2017.01.005.
Lam, N.T., Chollakup, R., Smitthipong, W., Nimchua, T., Sukyai, P., Characterization of cellulose nanocrystals extracted from sugarcane bagasse for potential biomedical materials. Sugar Tech, 19, 2017, 10.1007/s12355-016-0507-1.
Niamsap, T., Lam, N.T., Sukyai, P., Production of hydroxyapatite-bacterial nano- cellulose scaffold with assist of cellulose nanocrystals. Carbohydr. Polym., 205, 2019, 10.1016/j.carbpol.2018.10.034.
Ly, M., Mekonnen, T.H., Cationic surfactant modified cellulose nanocrystals for corrosion protective nanocomposite surface coatings. J. Ind. Eng. Chem., 83, 2020, 10.1016/j.jiec.2019.12.014.
Manimaran, M., Norizan, M.N., Mohamad Kassim, M.H., Adam, M.R., Norrrahim, M.N.F., Knight, V.F., Critical assessment of the thermal stability and degradation of chemically functionalized nanocellulose-based polymer nanocomposites. Nanotechnol. Rev., 13, 2024, 10.1515/ntrev-2024-0005.
D'Acierno, F., Capron, I., Modulation of surface properties of cellulose nanocrystals through adsorption of tannic acid and alkyl cellulose derivatives. Carbohydr. Polym., 319, 2023, 10.1016/j.carbpol.2023.121159.
Shi, X., Qin, X., Dai, Y., Liu, X., Wang, W., Zhong, J., Improved catalytic properties of Candida antarctica lipase B immobilized on cetyl chloroformate-modified cellulose nanocrystals. Int. J. Biol. Macromol., 220, 2022, 10.1016/j.ijbiomac.2022.08.170.
Esmizadeh, E., Gupta, A., Asrat, S., Mekonnen, T.H., Crystallization and performance evolution of PHBV nanocomposites through annealing: the role of surface modifi- cation of CNCs. Polymer, 308, 2024, 10.1016/j.polymer.2024.127352.
Wu, Q., Xu, J., Wu, Z., Zhu, S., Gao, Y., Shi, C., The effect of surface modification on chemical and crystalline structure of the cellulose III nanocrystals. Carbohydr. Polym., 235, 2020, 10.1016/j.carbpol.2020.115962.
Ávila Ramírez, J.A., Gómez Hoyos, C., Arroyo, S., Cerrutti, P., Foresti, M.L., Naturally occurring?-hydroxy acids: useful organocatalysts for the acetylation of cellulose nanofibres. Curr. Organocatal., 3, 2015, 28232503, 10.2174/22133372026661504.
Kang, H., Liu, R., Huang, Y., Graft modification of cellulose: methods, properties and applications. Polymer, 70, 2015, 10.1016/j.polymer.2015.05.041.
Liu, Z., Khurshid, K., Saldaña, M.D.A., Hydrogels and aerogels of cellulose nanofiber derived from barley straw with addition of chitosan using high-intensity ultrasound and supercritical CO2 drying. Ind. Crop. Prod., 216, 2024, 10.1016/j.indcrop.2024.118755.
Thirunavookarasu, N., Kumar, S., Shetty, P., Shanmugam, A., Rawson, A., Impact of ultrasound treatment on the structural modifications and functionality of carbo- hydrates – a review. Carbohydr. Res., 535, 2024, 10.1016/j.carres.2023.109017.
Costa, A.L.R., Gomes, A., Tibolla, H., Menegalli, F.C., Cunha, R.L., Cellulose nanofibers from banana peels as a Pickering emulsifier: high-energy emulsification processes. Carbohydr. Polym., 194, 2018, 10.1016/j.carbpol.2018.04.001.
Zhu, S., Sun, H., Mu, T., Li, Q., Richel, A., Preparation of cellulose nanocrystals from purple sweet potato peels by ultrasound-assisted maleic acid hydrolysis. Food Chem., 403, 2023, 10.1016/j.foodchem.2022.134496.
Tien Lam, N., Minh Quan, V., Boonrungsiman, S., Sukyai, P., Effectiveness of bio-dispersant in homogenizing hydroxyapatite for proliferation and differentiation of osteoblast. J. Colloid Interface Sci., 611, 2022, 10.1016/j.jcis.2021.12.088.
Lan, W., Zhang, X., Xu, M., Zhao, L., Huang, D., Wei, X., Chen, W., Carbon nanotube reinforced polyvinyl alcohol/biphasic calcium phosphate scaffold for bone tissue engineering. RSC Adv., 9, 2019, 10.1039/c9ra08569f.
Sukul, M., Sahariah, P., Lauzon, H.L., Borges, J., Másson, M., Mano, J.F., Haugen, H.J., Reseland, J.E., In vitro biological response of human osteoblasts in 3D chitosan sponges with controlled degree of deacetylation and molecular weight. Carbohydr. Polym., 254, 2021, 117434, 10.1016/j.carbpol.2020.117434.
Giubilini, A., Messori, M., Bondioli, F., Minetola, P., Iuliano, L., Nyström, G., Maniura-Weber, K., Rottmar, M., Siqueira, G., 3D-printed poly(3-hydroxybutyrate-co-3-hydroxyhexanoate)-cellulose-based scaffolds for biomedical applications. Biomacromolecules 24 (2023), 3961–3971, 10.1021/acs.biomac.3c00263.
Morsy, R., Development and characterization of antibacterial 3D porous hydroxyapatite-gelatin-PVA scaffolds containing zinc oxide nanoparticles. Mater. Chem. Phys., 314, 2024, 10.1016/j.matchemphys.2023.128831.
Ma, T., Hu, X., Lu, S., Cui, R., Zhao, J., Hu, X., Song, Y., Cellulose nanocrystals produced using recyclable sulfuric acid as hydrolysis media and their wetting molecular dynamics simulation. Int. J. Biol. Macromol. 184 (2021), 405–414, 10.1016/j.ijbiomac.2021.06.094.
Meirelles, A.A.D., Costa, A.L.R., Cunha, R.L., Cellulose nanocrystals from ultrasound process stabilizing O/W Pickering emulsion. Int. J. Biol. Macromol., 158, 2020, 10.1016/j.ijbiomac.2020.04.185.
Costa, A.L.R., Gomes, A., Furtado, G. de F., Tibolla, H., Menegalli, F.C., Cunha, R.L., Modulating in vitro digestibility of Pickering emulsions stabilized by food-grade polysaccharides particles. Carbohydr. Polym., 227, 2020, 10.1016/j.carbpol.2019.115344.
Lepetit, A., Drolet, R., Tolnai, B., Montplaisir, D., Zerrouki, R., Alkylation of micro- fibrillated cellulose – a green and efficient method for use in fiber-reinforced composites. Polymer, 2017, 10.1016/j.polymer.2017.08.024.
Nagarajan, K.J., Balaji, A.N., Rajan, S. Thanga Kasi, Basha, K. Sathick, Effect of sulfuric acid reaction time on the properties and behavior of cellulose nanocrystals from Cocos nucifera var-Aurantiaca peduncle's cellulose microfibers. Mater. Res. Express, 6, 2019, 10.1088/2053-1591/ab5a9d.
Jiang, H., Wu, S., Zhou, J., Preparation and modification of nanocellulose and its application to heavy metal adsorption: a review. Int. J. Biol. Macromol., 236, 2023, 10.1016/j.ijbiomac.2023.123916.
Guo, J., Guo, X., Wang, S., Yin, Y., Effects of ultrasonic treatment during acid hydrolysis on the yield, particle size and structure of cellulose nanocrystals. Carbohydr. Polym. 135 (2016), 248–255, 10.1016/j.carbpol.2015.08.068.
Lu, J., Askeland, P., Drzal, L.T., Surface modification of microfibrillated cellulose for epoxy composite applications. Polymer, 49, 2008, 10.1016/j.polymer.2008.01.028.
Shih, Y., Huang, C., Chen, P., Biodegradable green composites reinforced by the fiber recycling from disposable chopsticks. Mater. Sci. Eng., A 527 (2010), 1516–1521, 10.1016/j.msea.2009.10.024.
Chinta, M.L., Velidandi, A., Pabbathi, N.P.P., Dahariya, S., Parcha, S.R., Assessment of properties, applications and limitations of scaffolds based on cellulose and its deri- vatives for cartilage tissue engineering: a review. Int. J. Biol. Macromol., 175, 2021, 10.1016/j.ijbiomac.2021.01.196.
Li, K., Jin, S., Zhang, F., Zhou, Y., Zeng, G., Li, J., Shi, S.Q., Li, J., Bioinspired phenol-amine chemistry for developing bioadhesives based on biomineralized cellulose nanocrystals. Carbohydr. Polym., 296, 2022, 10.1016/j.carbpol.2022.119892.
Melikoğlu, A.Y., Bilek, S.E., Cesur, S., Optimum alkaline treatment parameters for the extraction of cellulose and production of cellulose nanocrystals from apple pomace. Carbohydr. Polym. 215 (2019), 330–337, 10.1016/j.carbpol.2019.03.103.
Wang, L., Li, Y., Ye, L., Zhi, C., Zhang, T., Miao, M., Unveiling structure and perfor- mance of tea-derived cellulose nanocrystals. Int. J. Biol. Macromol., 270, 2024, 10.1016/j.ijbiomac.2024.132117.
Roman, M., Winter, W.T., Effect of sulfate groups from sulfuric acid hydrolysis on the thermal degradation behavior of bacterial cellulose. Biomacromolecules, 5, 2004, 10.1021/bm034519+.
Torlopov, M.A., Martakov, I.S., Mikhaylov, V.I., Cherednichenko, K.A., Sitnikov, P., Synthesis and properties of thiol-modified CNC via surface tosylation. Carbohydr. Polym., 319, 2023, 10.1016/j.carbpol.2023.121169.
Shuai, C., Yang, W., Feng, P., Peng, S., Pan, H., Accelerated degradation of HAP/PLLA bone scaffold by PGA blending facilitates bioactivity and osteoconductivity. Bioact. Mater., 6, 2021, 10.1016/j.bioactmat.2020.09.001.
Bakkari, M., Bindiganavile, V., Boluk, Y., Facile synthesis of calcium hydroxide nanoparticles onto tempo-oxidized cellulose nanofibers for heritage conservation. ACS Omega, 4, 2019, 10.1021/acsomega.9b02643.
Deb, P., Das Lala, S., Barua, E., Deoghare, A.B., Physico-mechanical and biological analysis of composite bone scaffold developed from catla catla fish scale derived hydroxyapatite for bone tissue engineering. Arab. J. Sci. Eng., 49, 2024, 10.1007/s13369-023-07872-z.
Zhang, L., Lu, T., He, F., Zhang, W., Yuan, X., Wang, X., Ye, J., Physicochemical and cytological properties of poorly crystalline calcium-deficient hydroxyapatite with different ca/P ratios. Ceram. Int., 48, 2022, 10.1016/j.ceramint.2022.05.126.
Li, R., Fei, J., Cai, Y., Li, Y., Feng, J., Yao, J., Cellulose whiskers extracted from mulberry: a novel biomass production. Carbohydr. Polym. 76:1 (2009), 94–99, 10.1016/j.carbpol.2008.09.034.
Daldiken, E., Koçak, F.Z., Küçükdeveci, N., Synthesis and characterizations of clinoptilolite enriched hydroxyapatite nanoceramics by sol-gel route for bone regeneration. Ceram. Int., 50, 2024, 10.1016/j.ceramint.2024.03.084.
Abden, M.J., Afroze, J.D., Alam, M.S., Bahadur, N.M., Pressure less sintering and mechanical properties of hydroxyapatite/functionalized multi-walled carbon nanotube composite. Mater. Sci. Eng. C, 67, 2016, 10.1016/j.msec.2016.05.018.
Shuai, C., Peng, B., Feng, P., Yu, L., Lai, R., Min, A., In situ synthesis of hydroxy- apatite nanorods on graphene oxide nanosheets and their reinforcement in biopolymer scaffold. J. Adv. Res., 35, 2022, 10.1016/j.jare.2021.03.009.
Shuai, C., Shi, X., Wang, K., Gu, Y., Yang, F., Feng, P., Ag-doped CNT/HAP nanohybrids in a PLLA bone scaffold show significant antibacterial activity. Biodes. Manuf., 7, 2024, 10.1007/s42242-023-00264-0.
Avella, M., Cocca, M., Errico, M.E., Gentile, G., Polyvinyl alcohol biodegradable foams containing cellulose fibers. J. Cell. Plast., 2012, 10.1177/0021955X1244 9639.
Ma, P., Wu, W., Wei, Y., Ren, L., Lin, S., Wu, J., Biomimetic gelatin/chitosan/polyvinyl alcohol/nano-hydroxyapatite scaffolds for bone tissue engineering. Mater. Des., 207, 2021, 10.1016/j.matdes.2021.109865.
Dong, S., Hirani, A.A., Colacino, K.R., Lee, Y.W., Roman, M., Cytotoxicity and cellular uptake of cellulose nanocrystals. Nano Life, 02, 2012, 10.1142/s1793 984412410061.
Osathanon, T., Giachelli, C.M., Somerman, M.J., Immobilization of alkaline phosphatase on microporous nanofibrous fibrin scaffolds for bone tissue engineering. Biomaterials, 30, 2009, 10.1016/j.biomaterials.2009.05.022.
Abdal-Hay, A., Sheikh, F.A., Lim, J.K., Air jet spinning of hydroxyapatite/poly(lactic acid) hybrid nanocomposite membrane mats for bone tissue engineering. Colloids Surf. B Biointerfaces, 102, 2013, 10.1016/j.colsurfb.2012.09.017.
Sun, X., Yang, X., Su, Y., Teng, M., Liao, J., Niu, A., Liang, X., Morphology improvement of sandblasted and acid-etched titanium surface and osteoblast attachment promotion by hydroxyapatite coating. Rare Metal Mater. Eng., 44, 2015, 10.1016/s1875-5372(15)30014-x.
Patel, D.K., Dutta, S.D., Hexiu, J., Ganguly, K., Lim, K.T., 3D-printable chitosan/silk fibroin/cellulose nanoparticle scaffolds for bone regeneration via M2 macrophage polarization. Carbohydr. Polym., 281, 2022, 10.1016/j.carbpol.2021.119077.
Prakash, J., Prema, D., Venkataprasanna, K.S., Balagangadharan, K., Selvamurugan, N., Venkatasubbu, G.D., Nanocomposite chitosan film containing graphene oxide/hydroxyapatite/gold for bone tissue engineering. Int. J. Biol. Macromol., 154, 2020, 10.1016/j.ijbiomac.2020.03.095.
Budiraharjo, R., Neoh, K.G., Kang, E.T., Hydroxyapatite-coated carboxymethyl chitosan scaffolds for promoting osteoblast and stem cell differentiation. J. Colloid Interface Sci., 366, 2012, 10.1016/j.jcis.2011.09.072.