Abstract
Boron (B), which is a beneficial bioactive element for human, has an increasing interest in tissue engineering for the last 5 years. However, the effective B concentration in cell culture is still unknown. The aim of the present study is to investigate in vitro osteogenic potential of mesenchymal stem cells, isolated from adipose tissue (AdMSCs), on boron containing 2D and 3D cell cultures. At first, the effects of B concentrations between 1 and 20 μg/mL were evaluated on the survival and osteogenic differentiation of AdMSCs cultured on 2D cell cultures. The 3D cultures were established by using chitosan (Ch) scaffolds prepared by freeze-drying and Ch scaffolds combined with hydroxyapatite (HAp) and B containing hydroxyapatite (B-HAp) that are produced by microwave-induced biomimetic method. The proliferation and osteogenic differentiation of AdMSCs on Ch, HAp/Ch and B-HAp/Ch scaffolds were investigated by in vitro cell culture studies. The results were evaluated with respect to cell viability, bone related ECM gene expressions, and cellular morphology. It was demonstrated that cellular functions of AdMSCs were enhanced by boron in both 2D and 3D cultures. Especially, B-HAp/Ch scaffolds, which have both osteoinductive and osteoconductive properties based on presence of B and HAp in its structure, promoted adhesion, proliferation and osteogenic differentiation of AdMSCs.
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References
Aliborzi G, Vahdati A, Mehrabani D, Hosseini SE, Tamadon A (2016) Isolation, characterization and growth kinetic comparison of bone marrow and adipose tissue mesenchymal stem cells of Guinea Pig. Int J Stem Cells 9:115–123. https://doi.org/10.15283/ijsc.2016.9.1.115
Apdik H, Doğan A, Demirci S, Aydın S, Şahin F (2015) Dose-dependent effect of boric acid on myogenic differentiation of human adipose-derived stem cells (hADSCs). Biol Trace Elem Res 165:123–130. https://doi.org/10.1007/s12011-015-0253-3
Asghari Sana F, Çapkın Yurtsever M, Kaynak Bayrak G, Tunçay EÖ, Kiremitçi AS, Gümüşderelioğlu M (2017) Spreading, proliferation and differentiation of human dental pulp stem cells on chitosan scaffolds immobilized with RGD or fibronectin. Cytotechnology 69:617–630. https://doi.org/10.1007/s10616-017-0072-9
Beşkardeş IG, Gümüşderelioğlu M (2009) Biomimetic apatite-coated PCL scaffolds: effect of surface nanotopography on cellular functions. J Bioact Compat Polym 24:507–524. https://doi.org/10.1177/0883911509349311
Bunnell BA, Flaat M, Gagliardi C, Patel B, Ripoll C (2008) Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45:115–120. https://doi.org/10.1016/j.ymeth.2008.03.006
Çapkın M, Çakmak S, Kurt FÖ, Gümüşderelioğlu M, Şen BH, Türk BT, Deliloğlu-Gürhan Sİ (2012) Random/aligned electrospun PCL/PCL-collagen nanofibrous membranes: comparison of neural differentiation of rat AdMSCs and BMSCs. Biomed Mater 7:045013. https://doi.org/10.1088/1748-6041/7/4/045013
Demirci S, Doğan A, Şişli B, Sahin F (2014) Boron increases the cell viability of mesenchymal stem cells after long-term cryopreservation. Cryobiology 68:139–146. https://doi.org/10.1016/j.cryobiol.2014.01.010
Demirtaş TT, Kaynak G, Gümüşderelioğlu M (2015) Bone-like hydroxyapatite precipitated from 10 × SBF-like solution by microwave irradiation. Mater Sci Eng, C 49:713–719. https://doi.org/10.1016/j.msec.2015.01.057
Doğan A, Demirci S, Çağlayan AB, Kılıç E, Günal MY, Uslu Ü, Cumbul A, Şahin F (2014) Sodium pentaborate pentahydrate and pluronic containing hydrogel increases cutaneous wound healing in vitro and in vivo. Biol Trace Elem Res 162:72–79. https://doi.org/10.1007/s12011-014-0104-7
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Dj Prockop, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8:315–317. https://doi.org/10.1080/14653240600855905
Gorustovich AA, López JMP, Guglielmotti MB, Cabrini RL (2006) Biological performance of boron-modified bioactive glass particles implanted in rat tibia bone marrow. Biomed Mater 1:100–105. https://doi.org/10.1088/1748-6041/1/3/002
Gümüşderelioğlu M, Tunçay EÖ, Kaynak G, Demirtaş TT, Aydın ST, Hakkı SS (2015) Encapsulated boron as an osteoinductive agent for bone scaffolds. J Trace Elem Med Biol 31:120–128. https://doi.org/10.1016/j.jtemb.2015.03.008
Hakki SS, Bozkurt BS, Hakki EE (2010) Boron regulates mineralized tissue-associated proteins in osteoblasts (MC3T3-E1). J Trace Elem Med Biol 24:243–250. https://doi.org/10.1016/j.jtemb.2010.03.003
Hunt CD (2012) Dietary boron: progress in establishing essential roles in human physiology. J Trace Elem Med Biol 26:157–160. https://doi.org/10.1016/j.jtemb.2012.03.014
Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, Gimble JM, Bunnell BA (2006) Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99:1285–1297. https://doi.org/10.1002/jcb.20904
Kaynak Bayrak G, Demirtaş TT, Gümüşderelioğlu M (2017) Microwave-induced biomimetic approach for hydroxyapatite coatings of chitosan scaffolds. Carbohydr Polym 157:803–813. https://doi.org/10.1016/j.carbpol.2016.10.016
Kern S, Eichler H, Stoeve J, Klüter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294–1301. https://doi.org/10.1634/stemcells.2005-0342
Movahedi Najafabadi B, Abnosi MH (2016) Boron induces early matrix mineralization via calcium deposition and elevation of alkaline phosphatase activity in differentiated rat bone marrow mesenchymal stem cells. Cell J 18:62–73
Nielsen FH (2014) Update on human health effects of boron. J Trace Elem Med Biol 28:383–387. https://doi.org/10.1016/j.jtemb.2014.06.023
Peng L, Jia Z, Yin X, Zhang X, Liu Y, Chen P, Ma K, Zhou C (2008) Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue. Stem Cells Dev 17:761–774. https://doi.org/10.1089/scd.2007.0217
Rada T, Rui RL, Gomes ME (2009) Adipose tissue-derived stem cells and their application in bone and cartilage tissue engineering. Tissue Eng Part B 15:113–125. https://doi.org/10.1089/ten.teb.2008.0423
Rodbell M (1964) The metabolism of isolated fat cells. Compr Physiol 239:375–380
Strem BM, Hicok KC, Zhu M, Wulur I, Alfonso Z, Schreiber RE, Fraser JK, Hedrick M (2005) Multipotential differentiation of adipose tissue-derived stem cells. The Keio J Med 54:132–141. https://doi.org/10.2302/kjm.54.132
Taşlı PN, Doğan A, Demirci S, Şahin F (2013) Boron enhances odontogenic and osteogenic differentiation of human tooth germ stem cells (hTGSCs) in vitro. Biol Trace Elem Res 153:419–427. https://doi.org/10.1007/s12011-013-9657-0
Tığlı RS, Karakeçili A, Gümüşderelioğlu M (2007) In vitro characterization of chitosan scaffolds: influence of composition and deacetylation degree. J Mater Sci Mater Med 18:1665–1674. https://doi.org/10.1007/s10856-007-3066-x
Tropel P, Noel D, Platet N, Legrand P, Benabid A-L, Berger F (2004) Isolation and characterisation of mesenchymal stem cells from adult mouse bone marrow. Exp Cell Res 295:395–406. https://doi.org/10.1016/j.yexcr.2003.12.030
Tunçay EÖ, Demirtaş TT, Gümüşderelioğlu M (2017) Microwave-induced production of boron-doped HAp (B-HAp) and B-HAp coated composite scaffolds. J Trace Elem Med Biol 40:72–81. https://doi.org/10.1016/j.jtemb.2016.12.005
Uluisik I, Karakaya HC, Koc A (2018) The importance of boron in biological systems. J Trace Elem Med Biol 45:156–162. https://doi.org/10.1016/j.jtemb.2017.10.008
Wang J-M, Gu Y, Pan C-J, Yın L-R (2017) Isolation, culture and identification of human adipose derived stem cells. Exp Ther Med 13:1039–1043. https://doi.org/10.3892/etm.2017.4069
Wu C, Miron R, Sculean A, Kaskel S, Doert T, Schulze R, Zhang Y (2011) Proliferation, differentiation and gene expression of osteoblasts in boron-containing associated with dexamethasone deliver from mesoporous bioactive glass scaffolds. Biomaterials 32:7068–7078. https://doi.org/10.1016/j.biomaterials.2011.06.009
Yeh H-Y, Liu B-H, Sieber M, Hsu SH (2014) Substrate-dependent gene regulation of self-assembled human MSC spheroids on chitosan membranes. BMC Genom 15:10. https://doi.org/10.1186/1471-2164-15-10
Ying X, Cheng S, Wang W, Lin Z, Chen Q, Zhang W, Kou D, Shen Y, Cheng X, Rompis FA, Peng L, Zhu LuC (2011) Effect of boron on osteogenic differentiation of human bone marrow stromal cells. Biol Trace Elem Res 144:306–315. https://doi.org/10.1007/s12011-011-9094-x
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Akdere, Ö.E., Shikhaliyeva, İ. & Gümüşderelioğlu, M. Boron mediated 2D and 3D cultures of adipose derived mesenchymal stem cells. Cytotechnology 71, 611–622 (2019). https://doi.org/10.1007/s10616-019-00310-9
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DOI: https://doi.org/10.1007/s10616-019-00310-9