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Composite Biodegradable Polymeric Matrix Doped With Halloysite Nanotubes for the Repair of Bone Defects in Dogs

Published online by Cambridge University Press:  01 January 2024

Ekaterina Naumenko*
Affiliation:
Institute of Fundamental Medicine and Biology, Kazan Federal University, Kreml uramı 18, Kazan, Republic of Tatarstan, Russian Federation 420008
Elena Zakirova
Affiliation:
Institute of Fundamental Medicine and Biology, Kazan Federal University, Kreml uramı 18, Kazan, Republic of Tatarstan, Russian Federation 420008
Ivan Guryanov
Affiliation:
Institute of Fundamental Medicine and Biology, Kazan Federal University, Kreml uramı 18, Kazan, Republic of Tatarstan, Russian Federation 420008
Farida Akhatova
Affiliation:
Institute of Fundamental Medicine and Biology, Kazan Federal University, Kreml uramı 18, Kazan, Republic of Tatarstan, Russian Federation 420008
Mikhail Sergeev
Affiliation:
Kazan State Academy of Veterinary Medicine, Siberian Tract, 35, Kazan, Republic of Tatarstan, Russian Federation 420074
Anastasia Valeeva
Affiliation:
Kazan State Academy of Veterinary Medicine, Siberian Tract, 35, Kazan, Republic of Tatarstan, Russian Federation 420074
Rawil Fakhrullin*
Affiliation:
Institute of Fundamental Medicine and Biology, Kazan Federal University, Kreml uramı 18, Kazan, Republic of Tatarstan, Russian Federation 420008
*
*E-mail address of corresponding authors: ekaterina.naumenko@gmail.com; kazanbio@gmail.com
*E-mail address of corresponding authors: ekaterina.naumenko@gmail.com; kazanbio@gmail.com

Abstract

The use, in veterinary practice, of a three-dimensional biopolymer matrix (based on chitosan, agarose, and gelatin and doped with halloysite nanotubes) as a vehicle for mesenchymal stem cells (MSCs) to repair bone defects is reported here. The nanocomposite, combined with allogenic adipose-derived stem cells, was suitable for the repair of bone defects in dogs when paired with standard surgery involving metal Kirshner wires. The absence of inflammatory reactions to biopolymer matrices with allogenic stem cells was revealed in the case of an animal prone to inflammatory and allergic reactions. In addition, positive dynamics in the fusion of chronic bone defects without rejection reactions was observed after using a biopolymer matrix with MSCs.

Type
Article
Copyright
Copyright © The Clay Minerals Society 2021

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Footnotes

This paper belongs to a special issue on ‘Clay Minerals in Health Applications’

References

Abdullayev, E., & Lvov, Y. (2013). Halloysite clay nanotubes as a ceramic “skeleton” for functional biopolymer composites with sustained drug release. Journal of Materials Chemistry B, 1, 28942903.CrossRefGoogle ScholarPubMed
Achili, T.-M., Meyer, J., & Morgan, J. R. (2012). Advances in the formation, use and understanding of multicellular spheroids. Expert Opinion on Biological Therapy, 12(10), 13471360.CrossRefGoogle Scholar
Akhatova, F., Danilushkina, A., Kuku, G., Saricam, M., Culha, M., & Fakhrullin, R. (2018a). Simultaneous intracellular detection of plasmonic and non-plasmonic nanoparticles using dark-field hyperspectral microscopy. Bulletin of the Chemical Society of Japan, 91(11), 16401645.CrossRefGoogle Scholar
Akhatova, F., Fakhrullina, G., Khakimova, E., & Fakhrullin, R. (2018b). Atomic force microscopy for imaging and nanomechanical characterisation of live nematode epicuticle: A comparative Caenorhabditis elegans and Turbatrix aceti study. Ultramicroscopy, 194, 4047.CrossRefGoogle ScholarPubMed
Alstrup, T., Eijken, M., Bohn, A. B., Møller, B., & Damsgaard, T. E. (2019). Isolation of adipose tissue-derived stem cells: enzymatic digestion in combination with mechanical distortion to increase adipose tissue-derived stem cell yield from human aspirated fat. Current Protocols in Stem Cell Biology, 48(1), e68.CrossRefGoogle ScholarPubMed
Athanasiou, K. A., Zhu, C., Lanctot, D. R., Agrawal, C. M., & Wang, X. (2000). Fundamentals of biomechanics in tissue engineering of bone. Tissue Engineering, 6, 361381.CrossRefGoogle ScholarPubMed
Bertesteanu, S., Chifiriuc, M. C., Grumezescu, A. M., Printza, A. G., Marie-Paule, T., Grumezescu, V., Michaela, V., Lazar, V., & Grigore, R. (2014). Biomedical applications of synthetic, biodegradable polymers for the development of anti-infective strategies. Current Medicinal Chemistry, 21(29), 33833390.CrossRefGoogle ScholarPubMed
Blokhuis, T. J. (2014). Bioresorbable bone graft substitutes. In Mallick, K. (Ed.), Bone Substitute Biomaterials. Woodhead Publishing Series in Biomaterials (pp. 8092). Elsevier.CrossRefGoogle Scholar
Cavalcanti, S. C., Pereira, C. L., Mazzonetto, R., de Moraes, M., & Moreira, R. W. (2008). Histological and histomorphometric analyses of calcium phosphate cement in rabbit calvaria. Journal of Cranio-Maxillofacial Surgery, 36, 354359.CrossRefGoogle ScholarPubMed
Cavallaro, G., Milioto, S., Konnova, S., Fakhrullina, G., Akhatova, F., Lazzara, G., Fakhrullin, R., & Lvov, Y. (2020). Halloysite/Keratin nanocomposite for human hair photoprotection coating. ACS Applied Materials & Interfaces, 12, 2434824362.CrossRefGoogle ScholarPubMed
Cho, J. S., Park, J. H., Kang, J. H., Kim, S. E., Park, I. H., & Lee, H. M. (2015). Isolation and characterization of multipotent mesenchymal stem cells in nasal polyps. Experimental Biology and Medicine (Maywood, N.J.), 240(2), 185193.CrossRefGoogle ScholarPubMed
Christensen, F. B., Dalstra, M., Sejling, F., Overgaard, S., & Bunger, C. (2000). Titanium-alloy enhances bone-pedicle screw fixation: Mechanical and histomorphometrical results of titanium-alloy versus stainless steel. European Spine Journal, 9, 97103.CrossRefGoogle ScholarPubMed
Cornell, C. N. (1999). Osteoconductive materials and their role as substitutes for autogenous bone grafts. Orthopedic Clinics of North America, 4, 591598.CrossRefGoogle Scholar
Curtis, R., Goldhahn, J., Schwyn, R., Regazzoni, P., & Suhm, N. (2005). Fixation principles in metaphyseal bone—A patent based review. Osteoporosis International, 16, S54–S64.CrossRefGoogle ScholarPubMed
de Silva, R. T., Pasbakhsh, P., Goh, K. L., Chai, S.-P., & Ismail, H. (2013). Physico-chemical characterisation of chitosan/halloysite composite membranes. Polymer Testing, 32, 265271.CrossRefGoogle Scholar
Derjaguin, B. V., Muller, V. M., & Toporov, Y. P. (1975). Effect of contact deformations on the adhesion of particles. Journal of Colloid and Interface Science, 53, 314326.CrossRefGoogle Scholar
Dimitriou, R., Jones, E., Mcgonagle, D., & Giannoudis, P. V. (2011). Bone regeneration: current concepts and future directions. BMC Medicine, 9, 66.CrossRefGoogle ScholarPubMed
Driessens, F. C., van Dijk, J. W., & Borggreven, J. M. (1978). Biological calcium phosphates and their role in the physiology of bone and dental tissues I. Composition and solubility of calcium phosphates. Calcified Tissue International, 26, 127137.CrossRefGoogle ScholarPubMed
Eppley, B. L., & Sadove, A. M. (1995). A comparison of resorbable and metallic fixation in healing of calvarial bone grafts. Plastic and Reconstructive Surgery, 96, 316322.CrossRefGoogle ScholarPubMed
Fakhrullina, G. I., Akhatova, F. S., Lvov, Y. M., & Fakhrullin, R. F. (2015). Toxicity of halloysite clay nanotubes in vivo: a Caenorhabditis elegans study. Environmental Science: Nano, 2, 5459.Google Scholar
Fakhrullina, G., Akhatova, F., Kibardina, M., Fokin, D., & Fakhrullin, R. (2017). Nanoscale imaging and characterization of Caenorhabditis elegans epicuticle using atomic force microscopy. Nanomedicine: Nanotechnology, Biology and Medicine, 13(2), 483491.CrossRefGoogle Scholar
Fakhrullina, G., Khakimova, E., Akhatova, F., Lazzara, G., Parisi, F., & Fakhrullin, R. F. (2019). Selective antimicrobial effects of curcumin@halloysite nanoformulation: a Caenorhabditis elegans study. ACS Applied Materials & Interfaces, 11(26), 2305023064.CrossRefGoogle ScholarPubMed
Glotov, A., Stavitskaya, A., Chudakov, Y., Ivanov, E., Huang, W., Vinokurov, V., Zolotukhina, A., Maximov, A., Karakhanov, E., & Lvov, Y. (2019). Mesoporous metal catalysts templated on clay nanotubes. Bulletin of the Chemical Society of Japan, 92(1), 6169.CrossRefGoogle Scholar
Goodrich, J. T., Sandler, A. L., & Tepper, O. (2012). A review of reconstructive materials for use in craniofacial surgery bone fixation materials, bone substitutes, and distractors. Child's Nervous System, 28, 15771588.CrossRefGoogle ScholarPubMed
Guryanov, I., Naumenko, E., Akhatova, F., Nigamatzyanova, L., & Fakhrullin, R. (2020). Selective cytotoxic activity of prodigiosin@halloysite nanoformulation. Frontiers in Bioengineering and Biotechnology, 8, 424.CrossRefGoogle ScholarPubMed
Heinz, W. F., & Hoh, J. H. (1999). Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope. Trends in Biotechnology, 17, 143150.CrossRefGoogle ScholarPubMed
Hertz, H. (1881). Über die Berührung fester elastischer Körper. Journal für die reine und angewandte Mathematik, 92, 156171.Google Scholar
Hutmacher, D., Hurzeler, M. B., & Schliephake, H. (1996). A review of material properties of biodegradable and bioresorbable polymers and devices for GTR and GBR applications. The International Journal of Oral & Maxillofacial Implants, 11, 667678.Google ScholarPubMed
Jia, X., Minami, K., Uto, K., Chang, A. C., Hill, J. P., Nakanishi, J., & Ariga, K. (2020). Adaptive liquid interfacially assembled protein nanosheets for guiding mesenchymal stem cell fate. Advanced Materials, 32, 1905942.CrossRefGoogle ScholarPubMed
Johnson, K. L., Kendall, K., & Roberts, A. D. (1971). Surface energy and the contact of elastic solids. Proceedings of the Royal Society of London A. Mathematical and Physical Sciences, 324, A324301–A324313.Google Scholar
Kulig, D., Zimoch-Korzycka, A., Jarmoluk, A., & Marycz, K. (2016). Study on alginate–chitosan complex formed with different polymers ratio. Polymers, 8(5), 167.CrossRefGoogle Scholar
Lin, R.-Z., & Chang, H.-Y. (2008). Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnology Journal, 3, 11721184.CrossRefGoogle ScholarPubMed
Liu, M., Wu, C., Jiao, Y., Xiong, S., & Zhou, C. (2013). Chitosan–halloysite nanotubes nanocomposite scaffolds for tissue engineering. Journal of Materials Chemistry B, 1, 20782089.CrossRefGoogle ScholarPubMed
Lo Furno, D., Graziano, A. C., Caggia, S., Perrotta, R. E., Tarico, M. S., Giuffrida, R., & Cardile, V. (2013). Decrease of apoptosis markers during adipogenic differentiation of mesenchymal stem cells from human adipose tissue. Apoptosis: an International Journal on Programmed Cell Death, 18(5), 578588.CrossRefGoogle ScholarPubMed
Marti, C., Imhoff, A. B., Bahrs, C., & Romero, J. (1997). Metallic versus bioabsorbable interference screw for fixation of bone-patellar tendon-bone autograft in arthroscopic anterior cruciate ligament reconstruction. A preliminary report. Knee Surgery, Sports Traumatology, Arthroscopy, 5, 217221.CrossRefGoogle Scholar
Meloan, S. N., & Puchtler, H. (1985). Chemical mechanisms of staining methods: von Kossa's technique: What von Kossa really wrote and a modified reaction for selective demonstration of inorganic phosphates. Journal of Histotechnology, 8(1), 1113.CrossRefGoogle Scholar
Middleton, J. C., & Tipton, A. J. (2000). Synthetic biodegradable polymers as orthopedic devices. Biomaterials, 21, 23352346.CrossRefGoogle ScholarPubMed
Naumenko, E. A., & Fakhrullin, R.F. (2017). Toxicological evaluation of clay nanomaterials and polymer-clay nanocomposites. In Lvov, Y. M., Guo, B., & Fakhrullin, R. F. (Eds.), Functional Polymer Composites with Nanoclays (pp. 399419). Royal Society of Chemistry.Google Scholar
Naumenko, E., & Fakhrullin, R. (2019). Halloysite nanoclay/biopolymers composite materials in tissue engineering. Biotechnology Journal, 14(12), 1900055.CrossRefGoogle ScholarPubMed
Naumenko, E. A., Guryanov, I. D., Yendluri, R., Lvov, Y. M., & Fakhrullin, R. F. (2016). Clay nanotube–biopolymer composite scaffolds for tissue engineering. Nanoscale, 8, 72577271.CrossRefGoogle ScholarPubMed
Okamoto, M., & John, B. (2013). Synthetic biopolymer nanocomposites for tissue engineering scaffolds. Progress in Polymer Science, 38, 14871503.CrossRefGoogle Scholar
Ou, Q., Huang, K., Fu, C., Huang, C., Fang, Y., Gu, Z., Wu, J., & Wang, Y. (2020). Nanosilver-incorporated halloysite nanotubes/gelatin methacrylate hybrid hydrogel with osteoimmunomodulatory and antibacterial activity for bone regeneration. Chemical Engineering Journal, 382, 123019.CrossRefGoogle Scholar
Pereira, H. F., Cengiz, I. F., Silva, F. S., Reis, R. L., & Oliveira, J. M. (2020). Scaffolds and coatings for bone regeneration. Journal of Materials Science: Materials in Medicine, 31(3), 27.Google ScholarPubMed
Planka, L., Gal, P., Kecova, H., Klima, J., Hlucilova, J., Filova, E., Amler, E., Krupa, P., Kren, L., Srnec, R., Urbanova, L., Lorenzova, J., & Necas, A. (2008). Allogeneic and autogenous transplantations of MSCs in treatment of the physeal bone bridge in rabbits. BMC Biotechnology, 8, 70.CrossRefGoogle ScholarPubMed
Rabie, A. B., Wong, R. W., & Hagg, U. (2000). Composite autogenous bone and demineralized bone matrices used to repair defects in the parietal bone of rabbits. British Journal of Oral and Maxillofacial Surgery, 38, 565570.CrossRefGoogle ScholarPubMed
Rozhina, E., Batasheva, S., Gomzikova, M., Naumenko, E., & Fakhrullin, R. (2019). Multicellular spheroids formation: The synergistic effects of halloysite nanoclay and cationic magnetic nanoparticles. Colloids and Surfaces A: Physicochemical and Engineering Aspects, 565, 1624.CrossRefGoogle Scholar
Rozhina, E., Panchal, A., Akhatova, F., Lvov, Y., & Fakhrullin, R. (2020). Cytocompatibility and cellular uptake of alkylsilanemodified hydrophobic halloysite nanotubes. Applied Clay Science, 185, 105371.CrossRefGoogle Scholar
Shall, G., Menosky, M., Decker, S., Nethala, P., Welchko, R., Leveque, X., Lu, M., Sandstrom, M., Hochgeschwender, U., Rossignol, J., & Dunbar, G. (2018). Effects of passage number and differentiation protocol on the generation of dopaminergic neurons from rat bone marrow-derived mesenchymal stem cells. International Journal of Molecular Sciences, 19(3), 720.CrossRefGoogle ScholarPubMed
Singh, R., Bhattacharya, B., Tomar, S. K., Singh, V., & Singh, P. K. (2017). Electrical, optical and electrophotochemical studies on agarose based biopolymer electrolyte towards dye sensitized solar cell application. Measurement, 102, 214219.CrossRefGoogle Scholar
Song, J., Jia, X., Minami, K., Hill, J. P., Nakanishi, J., Shrestha, L. K., & Ariga, K. (2020). Large-area aligned fullerene nanocrystal scaffolds as culture substrates for enhancing mesenchymal stem cell self-renewal and multipotency. ACS Applied Nano Materials, 3, 64976506.CrossRefGoogle Scholar
Sun, X. M., Zhang, Y. H., Shen, B., & Jia, N. Q. (2010). Direct electrochemistry and electrocatalysis of horseradish peroxidase based on halloysite nanotubes/chitosan nanocomposite film. Electrochimica Acta, 56(2), 700705.CrossRefGoogle Scholar
Suner, S. S., Demirci, S., Yetiskin, B., Fakhrullin, R., Naumenko, E., Okay, O., Ayyala, R. S., & Sahiner, N. (2019). Cryogel composites based on hyaluronic acid and halloysite nanotubes as scaffold for tissue engineering. International Journal of Biological Macromolecules, 130, 627635.CrossRefGoogle ScholarPubMed
Tan, L., Yu, X., Wan, P., & Yang, K. (2013). Biodegradable materials for bone repairs: A review. Journal of Materials Science & Technology, 29, 503513.CrossRefGoogle Scholar
Tarasova, E., Naumenko, E., Rozhina, E., Akhatova, F., & Fakhrullin, F. (2019). Cytocompatibility and uptake of polycations-modified halloysite clay nanotubes. Applied Clay Science, 169, 2130.CrossRefGoogle Scholar
Ulery, B. D., Nair, L. S., & Laurencin, C. T. (2011). Biomedical applications of biodegradable polymers. Journal of Polymer Science Part B: Polymer Physics, 49, 832864.CrossRefGoogle ScholarPubMed
Wu, Z. Y., Sun, Q., Liu, M., Grottkau, B. E., He, Z. X., Zou, Q., & Ye, C. (2020). Correlation between the efficacy of stem cell therapy for osteonecrosis of the femoral head and cell viability. BMC Musculoskeletal Disorders, 21, 55.CrossRefGoogle ScholarPubMed
Wuisman, P. I., & Smit, T. H. (2006). Bioresorbable polymers: Heading for a new generation of spinal cages. European Spine Journal, 15, 133148.CrossRefGoogle ScholarPubMed
Yang, Y.-H. K., Ogando, C. R., Wang See, C., Chang, T.-Y., & Barabino, G. A. (2018). Changes in phenotype and differentiation potentialofhuman mesenchymal stem cells aging in vitro. Stem Cell Research & Therapy, 9, 131. https://doi.org/10.1186/s13287-018-0876-3CrossRefGoogle ScholarPubMed
Yendluri, R., Lvov, Y., de Villiers, M. M., Vinokurov, V., Naumenko, E., Tarasova, E., & Fakhrullin, R. (2017). Paclitaxel encapsulated in halloysite clay nanotubes for intestinal and intracellular delivery. Journal of Pharmaceutical Sciences, 106(10), 31313139.CrossRefGoogle ScholarPubMed
Zheng, Y., & Wang, A. (2010). Enhanced adsorption of ammonium using hydrogel composites based on chitosan and halloysite. Journal of Macromolecular Science Part A Pure and Applied Chemistry, 47(1), 3338.CrossRefGoogle Scholar