Abstract
The ideal construction and tissue substitute with adjusted characteristics and functionalities for the regeneration of bone defects are still under investigation. Current approaches have focused on the use of various biocompatible materials that have been synthesized with carbon-based materials with physicochemical characteristics that contribute to the differentiation of specific stem cell lineages. This work reports on the potential of poly-ε-caprolactone (PCL) membranes loaded with β-glycerol phosphate (β-GP) functionalized multiwall carbon nanotubes (f-MWCNTs) to induce differentiation of human dental pulp stem cells (HDPSCs) into osteoblasts. The HDPSCs were seeded on unmodified PCL + f-MWCNTs and β-GP decorated PCL + f-MWCNTs membranes, and then, physicochemical, mechanically and biologically characterized. It was observed an increase in the mechanical properties of PCL by MWCNTs addition rendering a more hydrophilic membrane those containing β-GP. Live/Dead and MTT cytotoxicity tests showed a higher number of living cells in PCL + f-MWCNTs + β-GP membranes, whereas von Kossa showed calcium deposits. After Wistar rat implantation, new bone formation was found around the critical size calvaria defects indicating that these membranes have the ability to enhance the osteodifferentiation of HDPSCs by increasing mineralization.
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References
Aboushady IM, Salem ZA, Sabry D, Mohamed A (2018) Comparative study of the osteogenic potential of mesenchymal stem cells derived from different sources. J Clin Exp Dent 10:e7–e13. https://doi.org/10.4317/jced.53957
Avilés F, Cauich-Rodríguez JV, Moo-Tah L, May-Pat A, Vargas-Coronado R (2009) Evaluation of mild acid oxidation treatments for MWCNT functionalization. Carbon 47:2970–2975. https://doi.org/10.1016/j.carbon.2009.06.044
Baker CE, Marvi T, Austin TM, Payne S, Mignemi ME, Gailani D, Wheeler AP, Nguyen TT, Lovejoy SA, Martus JE, Mencio GA, Schoenecker JG (2018) Dilutional coagulopathy in pediatric scoliosis surgery: a single center report. Pediatr Anesth 28:974–981. https://doi.org/10.1111/pan.13488
Barradas A, Yuan H, van Blitterswijk C, Habibovic P (2011) Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur Cells Mater 21:407–429. https://doi.org/10.22203/eCM.v021a31
Baykan E, Koc A, Eser Elcin A, Murat Elcin Y (2014) Evaluation of a biomimetic poly( ε -caprolactone)/β -tricalcium phosphate multispiral scaffold for bone tissue engineering: In vitro and in vivo studies. Biointerphases 9:029011. https://doi.org/10.1116/1.4870781
Birmingham E, Niebur GL, McHugh PE, Shaw G, Barry FP, McNamara LM (2012) Osteogenic differentiation of mesenchymal stem cells is regulated by osteocyte and osteoblast cells in a simplified bone niche. Eur Cell Mater 23:13–27
Bosi S, Ballerini L, Prato M (2013) Carbon nanotubes in tissue engineering. Top Curr Chem. https://doi.org/10.1007/128_2013_474
Caeiro JR, González P, Guede D (2013) Biomecánica y hueso (y II): ensayos en los distintos niveles jerárquicos del hueso y técnicas alternativas para la determinación de la resistencia ósea. Revista de Osteoporosis y Metabolismo Mineral 5:99–108. https://doi.org/10.4321/S1889-836X2013000200007
Das K, Madhusoodan A, Mili B, Kumar A, Saxena A, Kumar K, Sarkar M, Singh P, Srivastava S, Bag S (2017) Functionalized carbon nanotubes as suitable scaffold materials for proliferation and differentiation of canine mesenchymal stem cells. Int J Nanomed 12:3235–3252. https://doi.org/10.2147/IJN.S122945
Flores-Cedillo ML, Alvarado-Estrada KN, Pozos-Guillén AJ, Murguía-Ibarra JS, Vidal MA, Cervantes-Uc JM, Rosales-Ibáñez R, Cauich-Rodríguez JV (2016) Multiwall carbon nanotubes/polycaprolactone scaffolds seeded with human dental pulp stem cells for bone tissue regeneration. J Mater Sci Mater Med. https://doi.org/10.1007/s10856-015-5640-y
Fujii M, Matano M, Toshimitsu K, Takano A, Mikami Y, Nishikori S, Sugimoto S, Sato T (2018) Human intestinal organoids maintain self-renewal capacity and cellular diversity in niche-inspired culture condition. Cell Stem Cell 23:787-793.e6. https://doi.org/10.1016/j.stem.2018.11.016
Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81:531–535. https://doi.org/10.1177/154405910208100806
Guzmán-Uribe D, Estrada KNA, de Guillén AJP, Pérez SM, Ibáñez RR (2012) Development of a three-dimensional tissue construct from dental human ectomesenchymal stem cells: in vitro and in vivo study. Open Dent J 6:226–234. https://doi.org/10.2174/1874210601206010226
Haniu H, Saito N, Matsuda Y, Tsukahara T, Usui Y, Narita N, Hara K, Aoki K, Shimizu M, Ogihara N, Takanashi S, Okamoto M, Kobayashi S, Ishigaki N, Nakamura K, Kato H (2012) Basic potential of carbon nanotubes in tissue engineering applications [WWW Document]. J Nanomater. https://doi.org/10.1155/2012/343747
Huang B, Vyas C, Roberts I, Poutrel Q-A, Chiang W-H, Blaker JJ, Huang Z, Bártolo P (2019) Fabrication and characterisation of 3D printed MWCNT composite porous scaffolds for bone regeneration. Mater Sci Eng C 98:266–278. https://doi.org/10.1016/j.msec.2018.12.100
Javanmard A, Mohammadi F, Mojtahedi H (2020) Reconstruction of a total rhinectomy defect by implant-retained nasal prosthesis: a clinical report. Oral Maxillofac Surg Cases 6:100141. https://doi.org/10.1016/j.omsc.2020.100141
Kang E-S, Kim D-S, Suhito IR, Choo S-S, Kim S-J, Song I, Kim T-H (2017) Guiding osteogenesis of mesenchymal stem cells using carbon-based nanomaterials. Nano Converg. https://doi.org/10.1186/s40580-017-0096-z
Khan WS, Rayan F, Dhinsa BS, Marsh D (2012) An osteoconductive, osteoinductive, and osteogenic tissue-engineered product for trauma and orthopaedic surgery: how far are we? [WWW Document]. Stem Cells International. https://doi.org/10.1155/2012/236231
Kiang JD, Wen JH, del Álamo JC, Engler AJ (2013) Dynamic and reversible surface topography influences cell morphology. J Biomed Mater Res 101A:2313–2321. https://doi.org/10.1002/jbm.a.34543
Knight MN, Hankenson KD (2013) Mesenchymal stem cells in bone regeneration. Adv Wound Care 2:306–316. https://doi.org/10.1089/wound.2012.0420
Krawetz RJ, Taiani JT, Wu YE, Liu S, Meng G, Matyas JR, Rancourt DE (2011) Collagen I scaffolds cross-linked with beta-glycerol phosphate induce osteogenic differentiation of embryonic stem cells in vitro and regulate their tumorigenic potential in vivo. Tissue Eng Part A 18:1014–1024. https://doi.org/10.1089/ten.tea.2011.0174
Langenbach F, Handschel J (2013) Effects of dexamethasone, ascorbic acid and β-glycerophosphate on the osteogenic differentiation of stem cells in vitro. Stem Cell Res Ther 4:117. https://doi.org/10.1186/scrt328
Lee H-S, Kang J-I, Chung W-J, Lee DH, Lee BY, Lee S-W, Yoo SY (2018) Engineered phage matrix stiffness-modulating osteogenic differentiation. ACS Appl Mater Interfaces 10:4349–4358. https://doi.org/10.1021/acsami.7b17871
Lutolf MP, Gilbert PM, Blau HM (2009) Designing materials to direct stem-cell fate. Nature 462:433–441. https://doi.org/10.1038/nature08602
Martin-Del-Campo M, Rosales-Ibañez R, Alvarado K, Sampedro JG, Garcia-Sepulveda CA, Deb S, San Román J, Rojo L (2016) Strontium folate loaded biohybrid scaffolds seeded with dental pulp stem cells induce in vivo bone regeneration in critical sized defects. Biomater Sci 4:1596–1604. https://doi.org/10.1039/c6bm00459h
Matassi F, Nistri L, Chicon Paez D, Innocenti M (2011) New biomaterials for bone regeneration. Clin Cases Miner Bone Metab 8:21–24
Mooney E, Dockery P, Greiser U, Murphy M, Barron V (2008) Carbon nanotubes and mesenchymal stem cells: biocompatibility. Prolif Differ Nano Lett 8:2137–2143. https://doi.org/10.1021/nl073300o
Pan L, Pei X, He R, Wan Q, Wang J (2012) Multiwall carbon nanotubes/polycaprolactone composites for bone tissue engineering application. Colloids Surf B Biointerfaces 93:226–234. https://doi.org/10.1016/j.colsurfb.2012.01.011
Pei B, Wang W, Dunne N, Li X (2019) Applications of carbon nanotubes in bone tissue regeneration and engineering: superiority, concerns, current advancements, and prospects. Nanomaterials (Basel). https://doi.org/10.3390/nano9101501
Qin H-L, Leng J, Zhang W, Kantchev EAB (2018) DFT modelling of a diphosphane—N-heterocyclic carbene–Rh(I) pincer complex rearrangement: a computational evaluation of the electronic effects in C-P bond activation. Dalton Trans 47:2662–2669. https://doi.org/10.1039/C7DT04759B
Ravanbakhsh H, Bao G, Mongeau L (2020) Carbon nanotubes promote cell migration in hydrogels. Sci Rep 10:2543. https://doi.org/10.1038/s41598-020-59463-9
Saravanan S, Vimalraj S, Thanikaivelan P, Banudevi S, Manivasagam G (2019) A review on injectable chitosan/beta glycerophosphate hydrogels for bone tissue regeneration. Int J Biol Macromol 121:38–54. https://doi.org/10.1016/j.ijbiomac.2018.10.014
Schemitsch EH (2017) Size matters: defining critical in bone defect size! J Orthop Trauma 31:S20. https://doi.org/10.1097/BOT.0000000000000978
Shokrieh MM, Saeedi A, Chitsazzadeh M (2013) Mechanical properties of multi-walled carbon nanotube/polyester nanocomposites. J Nanostruct Chem 3:20. https://doi.org/10.1186/2193-8865-3-20
Sparks NRL, Martinez IKC, Soto CH, Zur Nieden NI (2018) Low osteogenic yield in human pluripotent stem cells associates with differential neural crest promoter methylation. Stem Cells 36:349–362. https://doi.org/10.1002/stem.2746
Wang C, Cao X, Zhang Y (2017) A novel bioactive osteogenesis scaffold delivers ascorbic acid, β-glycerophosphate, and dexamethasone in vivo to promote bone regeneration. Oncotarget 8:31612–31625. https://doi.org/10.18632/oncotarget.15779
Wang Z, Inuzuka H, Fukushima H, Wan L, Gao D, Shaik S, Sarkar FH, Wei W (2012) Emerging roles of the FBW7 tumour suppressor in stem cell differentiation. EMBO Rep 13:36–43. https://doi.org/10.1038/embor.2011.231
Xing W, Pourteymoor S, Mohan S (2011) Ascorbic acid regulates osterix expression in osteoblasts by activation of prolyl hydroxylase and ubiquitination-mediated proteosomal degradation pathway. Physiol Genom 43:749–757. https://doi.org/10.1152/physiolgenomics.00229.2010
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Flores-Cedillo, M.L., Rosales-Ibáñez, R., Martin-del-Campo-Fierro, M. et al. Evaluation of the osteoinductive potential of HDPSCs cultured on β-glycerol phosphate functionalized MWCNTs/PCL membranes for bone regeneration. Polym. Bull. 79, 7229–7243 (2022). https://doi.org/10.1007/s00289-021-03721-x
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DOI: https://doi.org/10.1007/s00289-021-03721-x