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Background: Complex graft bioengineering is an actual topic in bone defects’ repair. For those, different scaffolds may be seeded with mesenchymal stromal cells and growth / differentiation factors. The natural role of platelet factors in reparative processes justifies the possibility of its usage for mesenchymal stromal cell proliferation and differentiation into osteoblasts in vitro in terms of the scaffold-based bioengineering. To develop and evaluate in vitro biocompatibility and osteoconductivity of a complex biograft based on a bioorganic scaffold seeded with human bone marrow mesenchymal stromal cells and saturated with growth and differentiation factors of allogeneic platelet-rich plasma.
Results: The properties of viability and adhesion of human bone marrow mesenchymal stromal cells in four types of bioorganic scaffolds were evaluated with biochemical and immunomorphological methods. Scaffold with the least cytotoxicity was used as a basis for complex biograft formation, so as a carrier for cells and platelet-derived factors. Then, cell proliferation activity and osteogenic differentiation were estimated with biochemical, morphological, histochemical and molecular-biological methods. The study showed high viability of cells in all bioorganic scaffolds but the least cytotoxicity was the one based on xenogeneic collagen sponge. We also found that allogeneic platelet-rich plasma positively affects the proliferation and osteogenic differentiation of bone marrow mesenchymal stromal cells in a complex biograft in vitro.
Conclusions: The properties of the developed complex biograft characterize its biocompatibility and osteoconductivity and make it potentially suitable for regenerative medicine, particularly for reconstructive surgery of bone defects.
References
Kosmacheva SM, Danilkovich NN, Shchepen AV, et al. Effect of platelet release on osteogenic differentiation of human bone marrow mesenchymal stem cells [in Rus.]. Cellular Technologies in Biology and Medicine 2013;4:210-216. https://doi.org/10.1007/s10517-014-2396-1 PMid: 24771449
Deev RV, Isaev AA, Kochish AY, et al. Pathways for the development of cell technologies in bone surgery [in Russian]. Traumatology and orthopedics in Russia 2008;47(1):65-75.
Szpalski C, Sagebin F, Barbaro M, Warren SM 2013. The influence of environmental factors on bone tissue engineering. J Biomed Mater Res Part B 2013:101B:663–675. https://doi.org/10.1002/jbm.b.32849 PMid: 23165885
Wang W, Yeung KWK. Bone grafts and biomaterials substitutes for bone defect repair: A review. Bioactive Materials 2017;2(4):224-247. https://doi.org/10.1016/j.bioactmat.2017.05.007 PMid: 29744432
Polo-Corrales L, Latorre-Esteves M, Ramirez-Vick J. Scaffold design for bone regeneration. Journal of Nanoscience and Nanotechnology 2014;14(1):15-56. https://doi.org/10.1166/jnn.2014.9127 PMid: 24730250
Makarevich S, Mazurenko A, Krivorot K, et al. The use of autologous mesenchymal stem cells for the purpose of spinal fusion [in Russian]. Science and Innovation 2019;11:79-84. https://doi.org/10.29235/1818-9857-2019-11-79-84
Langenbach F, Handschel J. Effects of dexamethasone, ascorbic acid and ?-glycerophosphate on the osteogenic differentiation of stem cells in vitro. Stem Cell Research Therapy 2013;4(5):117. https://doi.org/10.1186/scrt328 PMid: 24073831
Hutchings G, Moncrieff L, Dompe C, et al. Bone regeneration, reconstruction and use of osteogenic cells; from basic knowledge, animal models to clinical trials. Journal of Clinical Medicine 2020;9(1):139. https://doi.org/10.3390/jcm9010139 PMid: 31947922
Filippi M, Born G, Chaaban M, et al. Natural polymeric scaffolds in bone regeneration. Frontiers in Bioengineering and Biotechnology 2020;8:474. https://doi.org/10.3389/fbioe.2020.00474 PMid: 32509754
Steinert AF, Rackwitz L, Gilbert F, et al. Concise review: The clinical application of mesenchymal stem cells for musculoskeletal regeneration: Current status and perspectives. Stem Cell Translation Medicine 2012;1(3):237-247. https://doi.org/10.5966/sctm.2011-0036 PMid: 23197783
Correia C, Grayson WL, Park M, et al. In vitro model of vascularized bone: synergizing vascular development and osteogenesis. PLOS One 2011;6(12):e28352. https://doi.org/10.1371/journal.pone.0028352 PMid: 22164277
Ripamonti U, Crooks J, Rueger D. Induction of bone formation by recombinant human osteogenic protein-1 and sintered porous hydroxyapatite in adult primate. Plastic &Reconstructive Surgery 2001;107(4):977-988. https://doi.org/10.1097/00006534-200104010-00012 PMid: 11252092
Zhukova Y, Hiepen C, Knaus P, et al. The role of titanium surface nanostructuring on preosteoblast morphology, adhesion, and migration. Advanced Healthcare Materials 2017;6(15):1601244. https://doi.org/10.1002/adhm.201601244 PMid: 28371540
Garg T, Singh O, Arora S, et al. Scaffold: a novel carrier for cell and drug delivery. Critical Review in Therapeutic Drug Carrier Systems 2012;29(1):1–63. https://doi.org/10.1615/CritRevTherDrugCarrierSyst.v29.i1.10 PMid: 22356721
Seeherman H, Wozney J, Li R. Bone morphogenetic protein delivery systems. Spine 2002;27(16S):16-23. https://doi.org/10.1097/00007632-200208151-00005 PMid: 12205414
Oliveira JF, Aguiar PF, Rossi AM, et al. Effect of process parameters on the characteristics of porous calcium phosphate ceramics for bone tissue scaffolds. Artificial Organs 2003;27(5):406-411. https://doi.org/10.1046/j.1525-1594.2003.07247.x PMid: 12752198
Kruyt MC, van Gaalen SM, Oner FC, et al. Bone tissue engineering and spinal fusion: the potential of hybrid constructs by combining osteoprogenitor cells and scaffolds. Biomaterials 2004;25(9):1463-1473. https://doi.org/10.1016/S0142-9612(03)00490-3 PMid: 14697849
Neman J, Hambrecht A, Cadry C, et al. Stem cell-mediated osteogenesis: therapeutic potential for bone tissue engineering. Biologics: Targets and Therapy 2012;6:47-57. https://doi.org/10.2147/BTT.S22407 PMid: 22500114
Kitoh H, Kitakoji T, Tsuchiya H, et al. Transplantation of culture expanded bone marrow cells and platelet rich plasma in distraction osteogenesis of the long bones. Bone 2007;40(2):522-528. https://doi.org/10.1016/j.bone.2006.09.019 PMid: 17070744
Tsiklin LI, Pugachev EI, Kolsanov AV, et al. Biopolymer material from human spongiosa for regenerative medicine application. Polymers 2022;14(5):941. https://doi.org/10.3390/polym14050941 PMid: 35267766
Kim HN, Jiao A, Hwang AS, et al. Nanotopography-guided tissue engineering and regenerative medicine. Advanced Drug Delivery Reviews 2013;65(4):536–558. https://doi.org/10.1016/j.addr.2012.07.014 PMid: 22921841
Thurairajah K, Broadhead LM, Balogh ZJ. Trauma and stem cells: biology and potential therapeutic Implications. International Journal of Molecular Science 2017;18(3):577. https://doi.org/10.3390/ijms18030577 PMid: 28272352
Armiento AR, Hatt PL, Sanchez Rosenberg G, et al. Functional biomaterials for bone regeneration: a lesson in complex biology. Advanced Functional Materials 2020;30(44):1909874. https://doi.org/10.1002/adfm.201909874
Paladini F, Pollini M. Novel approaches and biomaterials for bone tissue engineering: a focus on silk fibroin. Materials 2022;15(19):6952. https://doi.org/10.3390/ma15196952 PMid: 36234293
Potapnev MP, Arabey AA, Kondratenko GG, et al. A soluble platelet-derived growth factors and regenerative medicine [In Russian]. Healthcare, 2014;9:32-40.
Marx RE, Carlson ER, Eichstaedt RM, et al. Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Oral Endodontology 1998;85(6):638-646. https://doi.org/10.1016/S1079-2104(98)90029-4 PMid: 9638695
Laquinta MR, Mazzoni E, Manfrini M, et al. Innovative biomaterials for bone regrowth. International Journal of Molecular Science 2019;20(3):618. https://doi.org/10.3390/ijms20030618 PMid: 30709008
Kollapan. Available online: https://collapan.ru/ [accessed 25 Aug 2023].
Osteomatrix. Available online: https://biostom.ru/info/articles/new/osteomatrix_osteomatriks_instruktsiya_k_primeneniyu/ [accessed 25 Aug 2023].
Lyostypt. Available online: https://catalogs.bbraun.com/en-01/p/PRID00000356/lyostypt-local-haemostatic-agent [accessed 25 Aug 2023].
Kotelnikov GP, Kolsanov AV, Volova L, et al. Technology of manufacturing of personalized reconstructive allogenic bone graft [in Russian.]. Khirurgiia 2019;3:65-72. https://doi.org/10.17116/hirurgia201903165 PMid: 30938359
World Health Organization. Blood Transfusion Safety Team. The Clinical use of blood: handbook. World Health Organization 2001;219 p. Available online: https://iris.who.int/handle/10665/42396 [accessed 25 Aug 2023]
Pierce J, Benedetti E, Preslar A, et al. Comparative analyses of industrial-scale human platelet lysate preparations. Transfusion 2017;57(12):2858-2869. https://doi.org/10.1111/trf.14324 PMid: 28990195
Shakhbazov AV, Goncharova NV, Kosmacheva SM, et al. Plasticity of human mesenchymal stem cell phenotype and expression profile under neurogenic conditions. Bulletin of Experimental Biology and Medicine (Cell Technologies in Biology and Medicine) 2009;147(4):513-516. https://doi.org/10.1007/s10517-009-0547-6 PMid: 19704961
Chen X, Huang J, Wu J, et al. Human mesenchymal stem cells. Cell Proliferation 2022;55(4):e13141. https://doi.org/10.1111/cpr.13141 PMid: 34936710
Schendzielorz P, Froelich K, Rak K, et al. Labeling adipose-derived stem cells with Hoechst 33342: usability and effects on differentiation potential and DNA damage. Stem Cells International 2016;2016:6549347. https://doi.org/10.1155/2016/6549347 PMid: 27375746
Danilkovich NN, Derkachev VS, Kosmacheva SM, et al. Application of bone-marrow mesenchymal stem cells and platelet-derived growth factors for human osteogenic graft engineering, 5th International conference on Tissue engineering and Regenerative Medicine, Berlin, Germany, 12-14 September, 2016:155. https://doi.org/10.4172/2157-7552.C1.025
Santos VH, Pfeifer JPh, Souza BJ, et al. Culture of mesenchymal stem cells derived from equine synovial membrane in alginate hydrogel microcapsules. BMC Veterinary Research 2018;14(1):114. https://doi.org/10.1186/s12917-018-1425-0 PMid: 29587733
Chevallier N, Anagnostou F, Zilber S, et al. Osteoblastic differentiation of human mesenchymal stem cells with platelet lysate. Biomaterials 2010;31(2):270-278. https://doi.org/10.1016/j.biomaterials.2009.09.043 PMid: 19783038
Kuvyrkov EV, Severin IN, Belyasova NA. Osteogenic differentiation of human bone marrow mesenchymal stem cells [in Russian]. News of the National Academy of Sciences of Belarus 2015;2:89-91.
Szustak M, Gendaszewska-Darmach E. Extracellular nucleotides selectively induce migration of chondrocytes and expression of type II collagen. International Journal of Molecular Sciences 2020;21(15):5227. https://doi.org/10.3390/ijms21155227 PMid: 32718031
Zhang D, Yi C, Qi S, et al. Effects of carbon nanotubes on the proliferation and differentiation of primary osteoblasts. Methods in Molecular Biology 2010;625:41-53. https://doi.org/10.1007/978-1-60761-579-8_5 PMid: 20422380
Meesuk L, Suwanprateeb J, Thammarakcharoen F, et al. Osteogenic differentiation and proliferation potentials of human bone marrow and umbilical cord-derived mesenchymal stem cells on the 3D-printed hydroxyapatite scaffolds. Scientific Reports 2022;12:19509. https://doi.org/10.1038/s41598-022-24160-2 PMid: 36376498
Janicki P, Boeuf S, Steck E, et al. Prediction of in vivo bone forming potency of bone marrow-derived human mesenchymal stem cells. European Cells and Materials 2011;21:488-507.
Yoon Y, Khan IU, Choi KU, et al. Different bone healing effects of undifferentiated and osteogenic differentiated mesenchymal stromal cell sheets in canine radial fracture model. Tissue Engineering and Regenerative Medicine 2018;15(1):115-124. https://doi.org/10.1007/s13770-017-0092-8 PMid: 30603539
Kuk M, Kim Y, Lee SH, et al. Osteogenic ability of canine adipose-derived mesenchymal stromal cell sheets in relation to culture time. Cell Transplantation 2015;25(7):1415-1422. https://doi.org/10.3727/096368915X689532 PMid: 26395978
Szpalski C, Barbaro M, Sagebin F, et al. Bone tissue engineering: Current strategies and techniques – Part II: Cell types. Tissue Engineering Part B: Reviews 2012;18(4):258-269. https://doi.org/10.1089/ten.teb.2011.0440 PMid: 22224439
Cao S, Zhao Y, Hu Y, et al. New perspectives: In situ tissue engineering for bone repair scaffold. Composites Part B: Engineering 2020;202:108445. https://doi.org/10.1016/j.compositesb.2020.108445
Abazari MF, Hosseini Z, Karizi SZ, et al. Different osteogenic differentiation potential of mesenchymal stem cells on three different polymeric substrates. Gene 2020;740:144534. https://doi.org/10.1016/j.gene.2020.144534 PMid: 32145328
Mirzaei A, Saburi E, Enderami SE, et al. Synergistic effects of polyaniline and pulsed electromagnetic field to stem cells osteogenic differentiation on polyvinylidene fluoride scaffold. Artificial Cells, Nanomedicine, and Biotechnology 2019;47(1):3058-3066. https://doi.org/10.1080/21691401.2019.1645154 PMid: 31339375
Zheng J, Xie Y, Yoshitomi T, et al. Stepwise proliferation and chondrogenic differentiation of mesenchymal stem cells in collagen sponges under different microenvironments. International Journal of Molecular Science 2022;23(12):6406. https://doi.org/10.3390/ijms23126406 PMid: 35742851
Kasten P, Vogel J, Beyen I, et al. Effect of platelet-rich plasma on the in vitro proliferation and osteogenic differentiation of human mesenchymal stem cells on distinct calcium phosphate scaffolds: the specific surface area makes a difference. Journal of Biomaterials Applications 2008;23(2):169-188. https://doi.org/10.1177/0885328207088269 PMid: 18632770
Kocaoemer A, Kern S, Kluter H, et al. Human AB serum and thrombin-activated platelet-rich plasma are suitable alternatives to fetal calf serum for the expansion of mesenchymal stem cells from adipose tissue. Stem Cells 2007;25:1270-1278. https://doi.org/10.1634/stemcells.2006-0627 PMid: 1725552
Borzini P, Mazzucco L. Tissue regeneration and in loco administration of platelet derivatives: clinical outcome, heterogeneous products, and heterogeneity of the effector mechanisms. Transfusion 2005;45(11):1759-1767. https://doi.org/10.1111/j.1537-2995.2005.00600.x PMid: 16271101
Krasilnikova OA, Baranovskii DS, Yakimova AO, et al. Intraoperative creation of Tissue-Engineered Grafts with Minimally Manipulated cells: new concept of bone tissue engineering in situ. Bioengineering 2022;9(11):704. https://doi.org/10.3390/bioengineering9110704 PMid: 36421105
Guven S, Karagianni M, Schwalbe M, et al. Validation of an automated procedure to isolate human adipose tissue–derived cells by using the Sepax® technology. Tissue Eng. Part C Methods 2012;18(8):575-582. https://doi.org/10.1089/ten.tec.2011.0617 PMid: 22372873
Ahn G, Lee JS, Yun WS, et al. Cleft alveolus reconstruction using a three-dimensional printed bioresorbable scaffold with human bone marrow cells. Journal of Craniofacial Surgery 2018;29(7):1880-1883. https://doi.org/10.1097/SCS.0000000000004747 PMid: 30028404
Shchanitsyn IN, Ivanov AN, Ulyanov VY, et al. Modern concepts of stimulation of bone tissue regeneration using biologically active scaffolds [in Russian]. Cytology 2019;61(1):16-34. https://doi.org/10.1134/S0041377119010061
Walsh DP, Raftery RM, Murphy R, et al. Gene activated scaffolds incorporating star-shaped polypeptide-pDNA nanomedicines accelerate bone tissue regeneration in vivo. Biomaterials of Science 2021;9:4984-4999. https://doi.org/10.1039/D1BM00094B PMid: 34086016
Presnyakov EV, Rochev ES, Tserceil VV, et al. Chondrogenesis induced in vivo by gene-activated hydrogel based on hyaluronic acid and plasmid DNA encoding VEGF. Genes and Cells 2021;16(2):47-53. https://doi.org/10.23868/202107005
Stamnitz S, Klimczak A. Mesenchymal stem cells, bioactive factors, and scaffolds in bone repair: from research perspectives to clinical practice. Cells 2021;10(8):1925. https://doi.org/10.3390/cells10081925 PMid: 34440694
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