The Effect of Boron-Containing Nano-Hydroxyapatite on Bone Cells.
Alkaline Phosphatase
/ metabolism
Biocompatible Materials
/ chemistry
Bone Regeneration
/ drug effects
Boron
/ chemistry
Cell Differentiation
/ drug effects
Cell Line, Tumor
Cell Proliferation
/ drug effects
Cells, Cultured
Drug Liberation
Durapatite
/ chemistry
Humans
Mesenchymal Stem Cells
/ drug effects
Nanocomposites
/ chemistry
Osteoblasts
/ drug effects
Bone
Boron
Mesenchymal stem cell
Nano-hydroxyapatite
SaOS-2
Transcriptome
Journal
Biological trace element research
ISSN: 1559-0720
Titre abrégé: Biol Trace Elem Res
Pays: United States
ID NLM: 7911509
Informations de publication
Date de publication:
Feb 2020
Feb 2020
Historique:
received:
09
12
2018
accepted:
27
03
2019
pubmed:
10
5
2019
medline:
9
6
2020
entrez:
10
5
2019
Statut:
ppublish
Résumé
Metabolic diseases or injuries damage bone structure and self-renewal capacity. Trace elements and hydroxyapatite crystals are important in the development of biomaterials to support the renewal of bone extracellular matrix. In this study, it was assumed that the boron-loaded nanometer-sized hydroxyapatite composite supports the construction of extracellular matrix by controlled boron release in order to prevent its toxic effect. In this context, boron release from nanometer-sized hydroxyapatite was calculated by ICP-MS as in large proportion within 1 h and continuing release was provided at a constant low dose. The effect of the boron-containing nanometer-sized hydroxyapatite composite on the proliferation of SaOS-2 osteoblasts and human bone marrow-derived mesenchymal stem cells was evaluated by WST-1 and compared with the effects of nano-hydroxyapatite and boric acid. Boron increased proliferation of mesenchymal stem cells at high doses and exhibited different effects on osteoblastic cell proliferation. Boron-containing nano-hydroxyapatite composites increased osteogenic differentiation of mesenchymal stem cells by increasing alkaline phosphatase activity, when compared to nano-hydroxyapatite composite and boric acid. The molecular mechanism of effective dose of boron-containing hydroxyapatite has been assessed by transcriptomic analysis and shown to affect genes involved in Wnt, TGF-β, and response to stress signaling pathways when compared to nano-hydroxyapatite composite and boric acid. Finally, a safe osteoconductive dose range of boron-containing nano-hydroxyapatite composites for local repair of bone injuries and the molecular effect profile in the effective dose should be determined by further studies to validation of the regenerative therapeutic effect window.
Identifiants
pubmed: 31069715
doi: 10.1007/s12011-019-01710-w
pii: 10.1007/s12011-019-01710-w
doi:
Substances chimiques
Biocompatible Materials
0
Durapatite
91D9GV0Z28
Alkaline Phosphatase
EC 3.1.3.1
Boron
N9E3X5056Q
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
364-376Subventions
Organisme : Hacettepe University Scientific Research Project Coordination Unit
ID : TBB-2017-13-312
Références
Kankilic B, Kose S, Korkusuz P, Timucin M, Korkusuz F (2016) Mesenchymal stem cells and Nano-bioceramics for bone regeneration. Curr Stem Cell Res Ther 11(6):487–493
doi: 10.2174/1574888X10666150202150518
Kankilic B, Dede EC, Korkusuz P, Timuçin M, Korkusuz F (2017) Apatites for orthopedic applications. Clinical Applications of Biomaterials. Springer, In, pp 65–90
Pascaretti-Grizon F, Guillaume B, Terranova L, Arbez B, Libouban H, Chappard D (2017) Maxillary sinus lift with Beta-Tricalcium phosphate (beta-TCP) in edentulous patients: a Nanotomographic and Raman study. Calcif Tissue Int 101(3):280–290. https://doi.org/10.1007/s00223-017-0280-5
doi: 10.1007/s00223-017-0280-5
pubmed: 28447119
Ciftci E, Köse S, Korkusuz P, Timuçin M, Korkusuz F (2014) Boron containing Nano hydroxyapatites (Bn-HAp) stimulate mesenchymal stem cell adhesion, proliferation and differentiation. Key Eng Mater 631:373–378
Bi L, Rahaman MN, Day DE, Brown Z, Samujh C, Liu X, Mohammadkhah A, Dusevich V, Eick JD, Bonewald LF (2013) Effect of bioactive borate glass microstructure on bone regeneration, angiogenesis, and hydroxyapatite conversion in a rat calvarial defect model. Acta Biomater 9(8):8015–8026. https://doi.org/10.1016/j.actbio.2013.04.043
doi: 10.1016/j.actbio.2013.04.043
pubmed: 23643606
Korkusuz F, Timuçin M, Korkusuz P (2014) Nanocrystalline apatite-based biomaterials and stem cells in Orthopaedics. In: Ben-Nissan B (ed) Advances in calcium phosphate biomaterials. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 373–390. https://doi.org/10.1007/978-3-642-53980-0_12
doi: 10.1007/978-3-642-53980-0_12
Dessordi R, Spirlandeli AL, Zamarioli A, Volpon JB, Navarro AM (2017) Boron supplementation improves bone health of non-obese diabetic mice. J Trace Elem Med Biol 39:169–175. https://doi.org/10.1016/j.jtemb.2016.09.011
doi: 10.1016/j.jtemb.2016.09.011
pubmed: 27908411
Cheng J, Peng K, Jin E, Zhang Y, Liu Y, Zhang N, Song H, Liu H, Tang Z (2011) Effect of additional boron on tibias of African ostrich chicks. Biol Trace Elem Res 144(1–3):538–549. https://doi.org/10.1007/s12011-011-9024-y
doi: 10.1007/s12011-011-9024-y
pubmed: 21461669
Hunt CD (2012) Dietary boron: progress in establishing essential roles in human physiology. J Trace Elem Med Biol 26(2–3):157–160. https://doi.org/10.1016/j.jtemb.2012.03.014
doi: 10.1016/j.jtemb.2012.03.014
pubmed: 22658717
Kurtoğlu F, Kurtoğlu V, Celik I, Kececi T, Nizamlioğlu M (2005) Effects of dietary boron supplementation on some biochemical parameters, peripheral blood lymphocytes, splenic plasma cells and bone characteristics of broiler chicks given diets with adequate or inadequate cholecalciferol (vitamin D3) content. Br Poult Sci 46(1):87–96
doi: 10.1080/00071660400024001
Hakki SS, Malkoc S, Dundar N, Kayis SA, Hakki EE, Hamurcu M, Baspinar N, Basoglu A, Nielsen FH, Götz W (2015) Dietary boron does not affect tooth strength, micro-hardness, and density, but affects tooth mineral composition and alveolar bone mineral density in rabbits fed a high-energy diet. J Trace Elem Med Biol 29:208–215
doi: 10.1016/j.jtemb.2014.10.007
Boyacioglu O, Orenay-Boyacioglu S, Yildirim H, Korkmaz M (2018) Boron intake, osteocalcin polymorphism and serum level in postmenopausal osteoporosis. J Trace Elem Med Biol 48:52–56. https://doi.org/10.1016/j.jtemb.2018.03.005
doi: 10.1016/j.jtemb.2018.03.005
pubmed: 29773193
Calis M, Demirtas TT, Vatansever A, Irmak G, Sakarya AH, Atilla P, Ozgur F, Gumusderelioglu M (2017) A biomimetic alternative to synthetic hydroxyapatite: "boron-containing bone-like hydroxyapatite" precipitated from simulated body fluid. Ann Plast Surg 79(3):304–311. https://doi.org/10.1097/SAP.0000000000001072
doi: 10.1097/SAP.0000000000001072
pubmed: 28430676
Chen X, Zhao Y, Geng S, Miron RJ, Zhang Q, Wu C, Zhang Y (2015) In vivo experimental study on bone regeneration in critical bone defects using PIB nanogels/boron-containing mesoporous bioactive glass composite scaffold. Int J Nanomedicine 10:839
pubmed: 25653525
pmcid: 4309792
Dogan A, Demirci S, Bayir Y, Halici Z, Karakus E, Aydin A, Cadirci E, Albayrak A, Demirci E, Karaman A, Ayan AK, Gundogdu C, Sahin F (2014) Boron containing poly-(lactide-co-glycolide) (PLGA) scaffolds for bone tissue engineering. Mater Sci Eng C Mater Biol Appl 44:246–253. https://doi.org/10.1016/j.msec.2014.08.035
doi: 10.1016/j.msec.2014.08.035
pubmed: 25280703
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
doi: 10.1016/j.jtemb.2015.03.008
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(29):7068–7078. https://doi.org/10.1016/j.biomaterials.2011.06.009
doi: 10.1016/j.biomaterials.2011.06.009
pubmed: 21704367
Balasubramanian P, Grünewald A, Detsch R, Hupa L, Jokic B, Tallia F, Solanki AK, Jones JR, Boccaccini AR (2016) Ion release, hydroxyapatite conversion, and cytotoxicity of boron-containing bioactive glass scaffolds. Int J Appl Glas Sci 7(2):206–215
doi: 10.1111/ijag.12206
Li X, Wang X, Jiang X, Yamaguchi M, Ito A, Bando Y, Golberg D (2016) Boron nitride nanotube-enhanced osteogenic differentiation of mesenchymal stem cells. J Biomed Mater Res B Appl Biomater 104(2):323–329. https://doi.org/10.1002/jbm.b.33391
doi: 10.1002/jbm.b.33391
pubmed: 25766516
Lu X, Li K, Xie Y, Huang L, Zheng X (2016) Chemical stability and osteogenic activity of plasma-sprayed boron-modified calcium silicate-based coatings. J Mater Sci Mater Med 27(11):166. https://doi.org/10.1007/s10856-016-5781-7
doi: 10.1007/s10856-016-5781-7
pubmed: 27663224
Tuncay EO, Demirtas TT, Gumusderelioglu 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
doi: 10.1016/j.jtemb.2016.12.005
pubmed: 28159225
Arslan A, Cakmak S, Gumusderelioglu M (2018) Enhanced osteogenic activity with boron-doped nanohydroxyapatite-loaded poly (butylene adipate-co-terephthalate) fibrous 3D matrix. Artif Cells Nanomed Biotechnol:1–10. https://doi.org/10.1080/21691401.2018.1470522
Hakki SS, Bozkurt BS, Hakki EE (2010) Boron regulates mineralized tissue-associated proteins in osteoblasts (MC3T3-E1). J Trace Elem Med Biol 24(4):243–250. https://doi.org/10.1016/j.jtemb.2010.03.003
doi: 10.1016/j.jtemb.2010.03.003
pubmed: 20685097
Ying X, Cheng S, Wang W, Lin Z, Chen Q, Zhang W, Kou D, Shen Y, Cheng X, Rompis FA, Peng L, Zhu Lu C (2011) Effect of boron on osteogenic differentiation of human bone marrow stromal cells. Biol Trace Elem Res 144(1–3):306–315. https://doi.org/10.1007/s12011-011-9094-x
doi: 10.1007/s12011-011-9094-x
pubmed: 21625915
Movahedi Najafabadi BA, 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(1):62–73
pubmed: 27054120
pmcid: 4819387
Yin C, Jia X, Miron RJ, Long Q, Xu H, Wei Y, Wu M, Zhang Y, Li Z (2018) Setd7 and its contribution to boron-induced bone regeneration in boron-mesoporous bioactive glass scaffolds. Acta Biomater 73:522–530. https://doi.org/10.1016/j.actbio.2018.04.033
doi: 10.1016/j.actbio.2018.04.033
pubmed: 29684621
Atila A, Halici Z, Cadirci E, Karakus E, Palabiyik SS, Ay N, Bakan F, Yilmaz SJMS, C E (2016) Study of the boron levels in serum after implantation of different ratios nano-hexagonal boron nitride–hydroxy apatite in rat femurs 58:1082–1089
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4):315–317. https://doi.org/10.1080/14653240600855905
doi: 10.1080/14653240600855905
pubmed: 16923606
Goncu Y, Gecgin M, Bakan F, Ay N (2017) Electrophoretic deposition of hydroxyapatite-hexagonal boron nitride composite coatings on Ti substrate. Mater Sci Eng C Mater Biol Appl 79:343–353. https://doi.org/10.1016/j.msec.2017.05.023
doi: 10.1016/j.msec.2017.05.023
pubmed: 28629027
Gautam C, Chakravarty D, Gautam A, Tiwary CS, Woellner CF, Mishra VK, Ahmad N, Ozden S, Jose S, Biradar S, Vajtai R, Trivedi R, Galvao DS, Ajayan PM (2018) Synthesis and 3D interconnected nanostructured h-BN-based biocomposites by low-temperature plasma sintering: bone regeneration applications. ACS Omega 3(6):6013–6021. https://doi.org/10.1021/acsomega.8b00707
doi: 10.1021/acsomega.8b00707
pubmed: 30023937
pmcid: 6045471
Shuai C, Gao C, Feng P, Xiao T, Yu K, Deng Y, Peng S (2016) Boron nitride nanotubes reinforce Tricalcium phosphate scaffolds and promote the osteogenic differentiation of mesenchymal stem cells. J Biomed Nanotechnol 12(5):934–947
doi: 10.1166/jbn.2016.2224
Nagarajan S, Belaid H, Pochat-Bohatier C, Teyssier C, Iatsunskyi I, Coy E, Balme S, Cornu D, Miele P, Kalkura NS, Cavailles V, Bechelany M (2017) Design of Boron Nitride/gelatin electrospun nanofibers for bone tissue engineering. ACS Appl Mater Interfaces 9(39):33695–33706. https://doi.org/10.1021/acsami.7b13199
doi: 10.1021/acsami.7b13199
pubmed: 28891632
Unal S, Ekren N, Sengil AZ, Oktar FN, Irmak S, Oral O, Sahin YM, Kilic O, Agathopoulos S, Gunduz O (2017) Synthesis, characterization, and biological properties of composites of hydroxyapatite and hexagonal boron nitride. J Biomed Mater Res B Appl Biomater 106:2384–2392. https://doi.org/10.1002/jbm.b.34046
doi: 10.1002/jbm.b.34046
pubmed: 29168913
Yang X, Li Y, He W, Huang Q, Zhang R, Feng Q (2018) Hydroxyapatite/collagen coating on PLGA electrospun fibers for osteogenic differentiation of bone marrow mesenchymal stem cells. 106 (11):2863–2870. https://doi.org/10.1002/jbm.a.36475
Cha M, Lee KM, Lee JHJTe, medicine r (2018) Positive Effects of Bisphosphonates on Osteogenic Differentiation in Patient-Derived Mesenchymal Stem Cells for the Treatment of Osteoporosis 15 (4):467–475
Takahara T, Arai Y, Kono Y, Shibata H, Maki M (2018) A microtubule-associated protein MAP1B binds to and regulates localization of a calcium-binding protein ALG-2. Biochem Biophys Res Commun 497(2):492–498
doi: 10.1016/j.bbrc.2018.02.048
Bleicher F, Couble ML, Buchaille R, Farges JC, Magloire H (2001) New genes involved in odontoblast differentiation. Adv Dent Res 15:30–33. https://doi.org/10.1177/08959374010150010701
doi: 10.1177/08959374010150010701
pubmed: 12640735
Deng X, Liang LN, Zhu D, Zheng LP, Yu JH, Meng XL, Zhao YN, Sun XX, Pan TW, Liu YQ (2018) Wedelolactone inhibits osteoclastogenesis but enhances osteoblastogenesis through altering different semaphorins production. Int Immunopharmacol 60:41–49. https://doi.org/10.1016/j.intimp.2018.04.037
doi: 10.1016/j.intimp.2018.04.037
pubmed: 29702282
Kang S, Kumanogoh A Semaphorins in bone development, homeostasis, and disease. In: Seminars in cell & developmental biology, 2013. vol 3. Elsevier, pp 163–171
Zhang Y, Wang N, Ma J, Chen XC, Li Z, Zhao W (2016) Expression profile analysis of new candidate genes for the therapy of primary osteoporosis. Eur Rev Med Pharmacol Sci 20(3):433–440
pubmed: 26914116
Zhang Y, Yang TL, Li X, Guo Y (2015) Functional analyses reveal the essential role of SOX6 and RUNX2 in the communication of chondrocyte and osteoblast. Osteoporos Int 26(2):553–561. https://doi.org/10.1007/s00198-014-2882-3
doi: 10.1007/s00198-014-2882-3
pubmed: 25212673
Lamora A, Talbot J, Mullard M, Brounais-Le Royer B, Redini F, Verrecchia F (2016) TGF-β signaling in bone remodeling and osteosarcoma progression. J Clin Med 5(11). https://doi.org/10.3390/jcm5110096
Yano M, Inoue Y, Tobimatsu T, Hendy G, Canaff L, Sugimoto T, Seino S, Kaji H (2012) Smad7 inhibits differentiation and mineralization of mouse osteoblastic cells. Endocr J 59(8):653–662
doi: 10.1507/endocrj.EJ12-0022
Kobylewski SE (2017) Activation of the EIF2α/ATF4 and ATF6 pathways in DU-145 cells by boric acid at the concentration reported in men at the US mean boron intake. Biol Trace Element Res 176(2):278–293
doi: 10.1007/s12011-016-0824-y
Polge C, Aniort J, Armani A, Claustre A, Coudy-Gandilhon C, Tournebize C, Deval C, Combaret L, Bechet D, Sandri M, Attaix D, Taillandier D (2018) Erratum: Polge, C., et al. UBE2E1 Is Preferentially Expressed in the Cytoplasm of Slow-Twitch Fibers and Protects Skeletal Muscles from Exacerbated Atrophy upon Dexamethasone Treatment. Cells 2018, 7, 214. Cells 7 (12). https://doi.org/10.3390/cells7120242
Kim JH, Mukherjee A, Madhavan SM, Konieczkowski M, Sedor JR (2012) WT1-interacting protein (Wtip) regulates podocyte phenotype by cell-cell and cell-matrix contact reorganization. Am J Physiol Renal Physiol 302(1):F103–F115. https://doi.org/10.1152/ajprenal.00419.2011
doi: 10.1152/ajprenal.00419.2011
pubmed: 21900451
Henderson KA, Kobylewski SE, Yamada KE, Eckhert CD (2015) Boric acid induces cytoplasmic stress granule formation, eIF2α phosphorylation, and ATF4 in prostate DU-145 cells. Biometals 28(1):133–141
doi: 10.1007/s10534-014-9809-5
Czekanska EM, Stoddart MJ, Ralphs JR, Richards RG, Hayes JS (2014) A phenotypic comparison of osteoblast cell lines versus human primary osteoblasts for biomaterials testing. J Biomed Mater Res A 102(8):2636–2643. https://doi.org/10.1002/jbm.a.34937
doi: 10.1002/jbm.a.34937
pubmed: 23983015