Bifunctional tissue-engineered composite construct for bone regeneration: The role of copper and fibrin.
Cu
angiogenesis
bone tissue engineering
fibrin
osteogenesis
Journal
Journal of biomedical materials research. Part B, Applied biomaterials
ISSN: 1552-4981
Titre abrégé: J Biomed Mater Res B Appl Biomater
Pays: United States
ID NLM: 101234238
Informations de publication
Date de publication:
Jan 2024
Jan 2024
Historique:
revised:
07
11
2023
received:
06
05
2023
accepted:
29
11
2023
medline:
22
1
2024
pubmed:
22
1
2024
entrez:
22
1
2024
Statut:
ppublish
Résumé
Bifunctional tissue engineering constructs promoting osteogenesis and angiogenesis are essential for bone regeneration. Metal ion-incorporated scaffolds and fibrin encapsulation attract much attention due to low cost, nontoxicity, and tunable control over ion and growth factor release. Herein, we investigated the effect of Cu.nHA/Cs/Gel scaffold and fibrin encapsulation on osteogenic and angiogenic differentiation of Wharton's jelly mesenchymal stem cells (WJMSCs) in vitro and in vivo. Cu-laden scaffolds were synthesized using salt leaching/freeze drying and were characterized using standard techniques. WJMSCs were isolated from the human umbilical cord and characterized. WJMSCs with or without encapsulating in fibrin were seeded onto scaffolds, followed by differentiating into the osteogenic lineage for 7 and 21 days. Osteogenic and angiogenic differentiation were evaluated using real-time polymerase chain reaction, western blot, and Alizarin red staining. Then, scaffolds were implanted into critical-sized calvarial bone defects in rats and histological assessments were performed using hematoxylin/eosin, Masson's trichrome, and CD31 immunohistochemical staining at 4 and 12 weeks. The scaffolds had good physicochemical and biological characteristics suitable for cell attachment and growth. Cu and fibrin increased the expression of ALP, RUNX2, OCN, COLI, VEGF, and HIF1α in differentiated WJMSCs. Implanted scaffolds were also biocompatible and were integrated well with the host tissue. Increased collagen condensation, mineralization, and blood vessel formation were observed in Cu-laden scaffolds. The fibrin-encapsulated groups showed the highest collagen and cell densities, immune cell infiltration, and bone trabeculae. CD31-positive cell population increased with fibrin encapsulation and seeding onto Cu-laden scaffolds. Adding Cu to scaffolds and encapsulating cells in fibrin are promising methods that guide osteogenesis and angiogenesis cellular signaling, leading to better bone regeneration.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e35362Subventions
Organisme : Iran University of Medical Sciences
ID : 97-02-87-33-186
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Barnes GL, Kostenuik PJ, Gerstenfeld LC, Einhorn TA. Growth factor regulation of fracture repair. J Bone Miner Res. 1999;14:1805-1815. doi:10.1359/jbmr.1999.14.11.1805
Wang X, Ao Q, Tian X, et al. 3D bioprinting technologies for hard tissue and organ engineering. Materials. 2016;9:802. doi:10.3390/ma9100802
Grosso A, Burger MG, Lunger A, Schaefer DJ, Banfi A, Di Maggio N. It takes two to tango: coupling of angiogenesis and osteogenesis for bone regeneration. Front Bioeng Biotechnol. 2017;5:68. doi:10.3389/fbioe.2017.00068
Manescu A, Giuliani A, Mohammadi S, et al. Osteogenic potential of dualblocks cultured with human periodontal ligament stem cells: in vitro and synchrotron microtomography study. J Periodontal Res. 2016;51:112-124. doi:10.1111/jre.12289
Rahimi F, Ahmadkhani N, Goodarzi A, et al. Gelatin-based hydrogel functionalized with taurine moieties for in vivo skin tissue regeneration. Bio-Des Manuf. 2023;6(2023):284-297. doi:10.1007/s42242-022-00227-x
Jamalpoor Z, Mirzadeh H, Joghataei MT, Zeini D, Bagheri-Khoulenjani S, Nourani MR. Fabrication of cancellous biomimetic chitosan-based nanocomposite scaffolds applying a combinational method for bone tissue engineering. J Biomed Mater Res A. 2015;103:1882-1892. doi:10.1002/jbm.a.35320
Lin Z, Cao Y, Zou J, et al. Improved osteogenesis and angiogenesis of a novel copper ions doped calcium phosphate cement. Mater Sci Eng C. 2020;114:111032. doi:10.1016/j.msec.2020.111032
Bozorgi A, Khazaei M, Soleimani M, Jamalpoor Z. Application of nanoparticles in bone tissue engineering; a review on the molecular mechanisms driving osteogenesis. Biomater Sci. 2021;9:4541-4567. doi:10.1039/D1BM00504A
Tapiero H, Townsend DM, Tew KD. Trace elements in human physiology and pathology. Copper. Biomed Pharmacother. 2003;57:386-398. doi:10.1016/s0753-3322(03)00012-x
Rath SN, Brandl A, Hiller D, et al. Bioactive copper-doped glass scaffolds can stimulate endothelial cells in co-culture in combination with mesenchymal stem cells. PLoS One. 2014;9:e113319. doi:10.1371/journal.pone.0113319
Li Q, Yang Z, Wei Z, Li D, Luo Y, Kang P. Copper-lithium-doped nanohydroxyapatite modulates mesenchymal stem cells homing to treat glucocorticoids-related osteonecrosis of the femoral head. Front Bioeng Biotechnol. 2022;10:916562. doi:10.3389/fbioe.2022.916562
Bozorgi A, Mozafari M, Khazaei M, Soleimani M, Jamalpoor Z. Fabrication, characterization, and optimization of a novel copper-incorporated chitosan/gelatin-based scaffold for bone tissue engineering applications. Bioimpacts. 2022;12:233-246. doi:10.34172/bi.2021.23451
de la Puente P, Ludeña D. Cell culture in autologous fibrin scaffolds for applications in tissue engineering. Exp Cell Res. 2014;322:1-11. doi:10.1016/j.yexcr.2013.12.017
Khodakaram-Tafti A, Mehrabani D, Shaterzadeh-Yazdi H. An overview on autologous fibrin glue in bone tissue engineering of maxillofacial surgery. Dent Res J. 2017;14:79-86.
Creste CFZ, Orsi PR, Landim-Alvarenga FC, et al. Highly effective fibrin biopolymer scaffold for stem cells upgrading bone regeneration. Materials. 2020;13:2747. doi:10.3390/ma13122747
Pedram Rad Z, Mokhtari J, Abbasi M. Preparation and characterization of Calendula officinalis-loaded PCL/gum arabic nanocomposite scaffolds for wound healing applications. Iran Polym J. 2019;28:51-63. doi:10.1007/s13726-018-0674-x
Peter M, Ganesh N, Selvamurugan N, et al. Preparation and characterization of chitosan-gelatin/nanohydroxyapatite composite scaffolds for tissue engineering applications. Carbohydr Polym. 2010;80:687-694. doi:10.1016/j.carbpol.2009.11.050
Jamalpoor Z, Soleimani M, Taromi N, Asgari A. Comparative evaluation of morphology and osteogenic behavior of human Wharton's jelly mesenchymal stem cells on 2D culture plate and 3D biomimetic scaffold. J Cell Physiol. 2019;234:23123-23134. doi:10.1002/jcp.28876
Correia C, Grayson WL, Park M, et al. In vitro model of vascularized bone: synergizing vascular development and osteogenesis. PloS One. 2011;6:e28352. doi:10.1371/journal.pone.0028352
Babaei H, Alibabrdel M, Asadian S, Siavashi V, Jabarpour M, Nassiri SM. Increased circulation mobilization of endothelial progenitor cells in preterm infants with retinopathy of prematurity. J Cell Biochem. 2018;119:6575-6583. doi:10.1002/jcb.26777
Jabarpour M, Siavashi V, Asadian S, Babaei H, Jafari SM, Nassiri SM. Hyperbilirubinemia-induced pro-angiogenic activity of infantile endothelial progenitor cells. Microvasc Res. 2018;118:49-56. doi:10.1016/j.mvr.2018.02.005
Siavashi V, Nassiri SM, Rahbarghazi R, Vafaei R, Sariri R. ECM-dependence of endothelial progenitor cell features. J Cell Biochem. 2016;117:1934-1946. doi:10.1002/jcb.25492
Gritsch L, Maqbool M, Mouriño V, et al. Chitosan/hydroxyapatite composite bone tissue engineering scaffolds with dual and decoupled therapeutic ion delivery: copper and strontium. J Mater Chem B. 2019;7:6109-6124. ECM. doi:10.1039/C9TB00897G
Liu C, Fu X, Pan H, et al. Biodegradable Mg-Cu alloys with enhanced osteogenesis, angiogenesis, and long-lasting antibacterial effects. Sci Rep. 2016;6:27374. doi:10.1038/srep27374
Ji Yin Y, Zhao F, Feng Song X, De Yao K, Lu WW, Chiyan LJ. Preparation and characterization of hydroxyapatite/chitosan-gelatin network composite. J Appl Polym Sci. 2000;77:2929-2938. doi:10.1002/10974628(20000923)77:13<2929::AIDAPP16>3.0.CO;2-Q
Lu Y, Li L, Zhu Y, et al. Multifunctional copper-containing carboxymethyl chitosan/alginate scaffolds for eradicating clinical bacterial infection and promoting bone formation. ACS Appl Mater Interfaces. 2018;10:127-138. doi:10.1021/acsami.7b13750
Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26:5474-5491. doi:10.1016/j.biomaterials.2005.02.002
Ma H, Feng C, Chang J, Wu C. 3D-printed bioceramic scaffolds: from bone tissue engineering to tumor therapy. Acta Biomater. 2018;79:37-59. doi:10.1016/j.actbio.2018.08.026
Radwan-Pragłowska J, Janus Ł, Piątkowski M, Bogdał D, Matysek D. 3D hierarchical, nanostructured chitosan/PLA/HA scaffolds doped with TiO(2)/Au/Pt NPs with tunable properties for guided bone tissue engineering. Polymers. 2020;12:792. doi:10.3390/polym12040792
Mou P, Peng H, Zhou L, Li L, Li H, Huang Q. A novel composite scaffold of Cu-doped nano calcium-deficient hydroxyapatite/multi-(amino acid) copolymer for bone tissue regeneration. Int J Nanomedicine. 2019;14:3331-3343. doi:10.2147/ijn.s195316
Kartikasari N, Yuliati A, Listiana I, et al. Characteristic of bovine hydroxyapatite-gelatin-chitosan scaffolds as biomaterial candidate for bone tissue engineering. Paper presented at IEEE EMBS Conference on Biomedical Engineering and Sciences (IECBES). 2016. pp 623-626.
Price PA, Toroian D, Chan WS. Tissue-nonspecific alkaline phosphatase is required for the calcification of collagen in serum: a possible mechanism for biomineralization. J Biol Chem. 2009;284:4594-4604. doi:10.1074/jbc.M803205200
Alvarez Perez MA, Guarino V, Cirillo V, Ambrosio L. In vitro mineralization and bone osteogenesis in poly(ε-caprolactone)/gelatin nanofibers. J Biomed Mater Res A. 2012;100:3008-3019. doi:10.1002/jbm.a.34233
Qin X, Jiang Q, Miyazaki T, Komori T. Runx2 regulates cranial suture closure by inducing hedgehog, Fgf, Wnt and Pthlh signaling pathway gene expressions in suture mesenchymal cells. Hum Mol Genet. 2019;28:896-911. doi:10.1093/hmg/ddy386
Oh JH, Kim HJ, Kim TI, Baek JH, Ryoo HM, Woo KM. The effects of the modulation of the fibronectin-binding capacity of fibrin by thrombin on osteoblast differentiation. Biomaterials. 2012;33:4089-4099. doi:10.1016/j.biomaterials.2012.02.028
Rahman MS, Akhtar N, Jamil HM, Banik RS, Asaduzzaman SM. TGF-β/BMP signaling and other molecular events: regulation of osteoblastogenesis and bone formation. Bone Res. 2015;3:15005. doi:10.1038/boneres.2015.5
Li X, Yang H, Zhang Z, et al. Platelet-rich fibrin exudate promotes the proliferation and osteogenic differentiation of human periodontal ligament cells in vitro. Mol Med Rep. 2018;18:4477-4485. doi:10.3892/mmr.2018.9472
Poundarik AA, Diab T, Sroga GE, et al. Dilatational band formation in bone. Proc Natl Acad Sci USA. 2012;109:19178-19183. doi:10.1073/pnas.1201513109
Bailey S, Karsenty G, Gundberg C, Vashishth D. Osteocalcin and osteopontin influence bone morphology and mechanical properties. Ann N Y Acad Sci. 2017;1409:79-84. doi:10.1111/nyas.13470
Wang X, Zhang Y, Choukroun J, Ghanaati S, Miron RJ. Effects of an injectable platelet-rich fibrin on osteoblast behavior and bone tissue formation in comparison to platelet-rich plasma. Platelets. 2018;29:48-55. doi:10.1080/09537104.2017.1293807
Medeiros DM. Copper, iron, and selenium dietary deficiencies negatively impact skeletal integrity: a review. Exp Biol Med. 2016;241:1316-1322. doi:10.1177/1535370216648805
Dunwoodie SL. The role of hypoxia in development of the mammalian embryo. Dev Cell. 2009;17:755-773. doi:10.1016/j.devcel.2009.11.008
Stegen S, Carmeliet G. The skeletal vascular system-breathing life into bone tissue. Bone. 2018;115:50-58. doi:10.1016/j.bone.2017.08.022
Weng L, Boda SK, Teusink MJ, Shuler FD, Li X, Xie J. Binary doping of strontium and copper enhancing osteogenesis and angiogenesis of bioactive glass nanofibers while suppressing osteoclast activity. ACS Appl Mater Interfaces. 2017;9:24484-24496. doi:10.1021/acsami.7b06521
Li Y, Wang J, Wang Y, Du W, Wang S. Transplantation of copper-doped calcium polyphosphate scaffolds combined with copper (II) preconditioned bone marrow mesenchymal stem cells for bone defect repair. J Biomater Appl. 2018;32:738-753. doi:10.1177/0885328217739456
Martin F, Linden T, Katschinski DM, et al. Copper-dependent activation of hypoxia-inducible factor (HIF)-1: implications for ceruloplasmin regulation. Blood. 2005;105:4613-4619. doi:10.1182/blood-2004-10-3980
Zhang W, Chang Q, Xu L, et al. Graphene oxide-copper nanocomposite-coated porous CaP scaffold for vascularized bone regeneration via activation of Hif-1α. Adv Healthc Mater. 2016;5:1299-1309. doi:10.1002/adhm.201500824
Murakami J, Ishii M, Suehiro F, Ishihata K, Nakamura N, Nishimura M. Vascular endothelial growth factor-C induces osteogenic differentiation of human mesenchymal stem cells through the ERK and RUNX2 pathway. Biochem Biophys Res Commun. 2017;484:710-718. doi:10.1016/j.bbrc.2017.02.001
Marino L, Castaldi MA, Rosamilio R, et al. Mesenchymal stem cells from the Wharton's jelly of the human umbilical cord: biological properties and therapeutic potential. Int J Stem Cells. 2019;12:218-226. 10.15283/ijsc18034
Gérard C, Bordeleau LJ, Barralet J, Doillon CJ. The stimulation of angiogenesis and collagen deposition by copper. Biomaterials. 2010;31:824-831. doi:10.1016/j.biomaterials.2009.10.009
Stegen S, van Gastel N, Carmeliet G. Bringing new life to damaged bone: the importance of angiogenesis in bone repair and regeneration. Bone. 2015;70:19-27. doi:10.1016/j.bone.2014.09.017
Ferreira RS Jr, de Barros LC, Abbade LPF, et al. Heterologous fibrin sealant derived from snake venom: from bench to bedside-an overview. J Venom Anim Toxins Incl Trop Dis. 2017;23:21. doi:10.1186/s40409-017-0109-8
Wang H, Zhao S, Zhou J, et al. Evaluation of borate bioactive glass scaffolds as a controlled delivery system for copper ions in stimulating osteogenesis and angiogenesis in bone healing. J Mater Chem B. 2014;2:8547-8557. doi:10.1039/c4tb01355g