Chitosan-collagen 3d matrix mimics trabecular bone and regulates rankl-mediated paracrine cues of differentiated osteoblast and mesenchymal stem cells for bone marrow macrophage-derived osteoclastogenesis

Elango, J.; Saravanakumar, K.; Rahman, S. U.; Henrotin, Yves; Regenstein, J. M.; Wu, W.; Bao, B.

doi:10.3390/biom9050173

Article (Périodiques scientifiques)

Chitosan-collagen 3d matrix mimics trabecular bone and regulates rankl-mediated paracrine cues of differentiated osteoblast and mesenchymal stem cells for bone marrow macrophage-derived osteoclastogenesis

Elango, J.; Saravanakumar, K.; Rahman, S. U. et al.

2019 • In Biomolecules, 9 (5)

Peer reviewed vérifié par ORBi

Permalien
https://hdl.handle.net/2268/246782

DOI
10.3390/biom9050173

PubMed
31060346

Documents (1)Envoyer vers Détails Statistiques Bibliographie Publications similaires

Documents

Texte intégral

biomolecules-09-00173-v2.pdf

Postprint Éditeur (7.5 MB)

Télécharger

Tous les documents dans ORBi sont protégés par une licence d'utilisation.

Envoyer vers

RIS BibTex APA Chicago Permalink X Linkedin

Détails

Mots-clés :

Biomechanical properties; Bone homeostasis; Chitosan-composite 3D matrix; Mesenchymal stem cells; Osteoclast; Ovariectomized mice; RANKL; Rheological properties; Runx2

Résumé :

[en] Recent studies have identified the regulatory mechanism of collagen in bone ossification and resorption. Due to its excellent bio-mimicry property, collagen is used for the treatment of several bone and joint disease such as arthritis, osteoporosis, and osteopenia. In bone, the biological action of collagen is highly influenced by the interactions of other bone materials such as glycosaminoglycan and minerals. In view of the above perceptions, collagen was crosslinked with chitosan, hydroxyapatite (H), and chondroitin sulfate (Cs), to produce a natural bone-like 3D structure and to evaluate its effect on bone homeostasis using bone marrow mesenchymal stem cells, osteoblast, and bone marrow macrophages. The XRD and micro-CT data confirmed the arrangement of H crystallites in the chitosan-collagen-H-Cs (CCHCs) three-dimensional (3D)-matrix and the three-dimensional structure of the matrix. The stimulatory osteoblastogenic and exploitive osteoclastogenic activity of 3D-matrices were identified using differentiated osteoblasts and osteoclasts, respectively. Besides, osteogenic progenitor’s paracrine cues for osteoclastogenesis showed that the differentiated osteoblast secreted higher levels of RANKL to support osteoclastogenesis, and the effect was downregulated by the CCHCs 3D-matrix. From that, it was hypothesized that the morphology of the CCHCs 3D-matrix resembles trabecular bone, which enhances bone growth, limits bone resorption, and could be a novel biomaterial for bone tissue engineering. © 2019 by the authors. Licensee MDPI, Basel, Switzerland.

Disciplines :

Rhumatologie

Auteur, co-auteur :

Elango, J.; Department of Marine Bio-Pharmacology, College of Food Science and Technology, Shanghai Ocean University, Shanghai, 201306, China, Bone Biology and Disease Unit, St. Vincent’s Institute of Medical Research, Melbourne, VIC 3065, Australia

Saravanakumar, K.; Department of Medical Biotechnology, College of Biomedical Sciences, Kangwon National University, Chuncheon, Gangwon 24341, South Korea

Rahman, S. U.; Interdisciplinary Research Centre in Biomedical Materials (IRCBM), COMSATS University Islamabad, Lahore Campus, Islamabad, 45550, Pakistan

Henrotin, Yves ; Université de Liège - ULiège > Département des sciences de la motricité > Unité de recherche sur l'os et le cartilage (U.R.O.C.)

Regenstein, J. M.; Department of Food Science, Cornell University, Ithaca, NY 14853-7201, United States

Wu, W.; Department of Marine Bio-Pharmacology, College of Food Science and Technology, Shanghai Ocean University, Shanghai, 201306, China

Bao, B.; Department of Marine Bio-Pharmacology, College of Food Science and Technology, Shanghai Ocean University, Shanghai, 201306, China

Langue du document :

Anglais

Titre :

Date de publication/diffusion :

2019

Titre du périodique :

Biomolecules

eISSN :

2218-273X

Maison d'édition :

MDPI

Volume/Tome :

Fascicule/Saison :

Peer reviewed :

Peer reviewed vérifié par ORBi

Organisme subsidiant :

NSCF - National Natural Science Foundation of China

Disponible sur ORBi :

depuis le 22 avril 2020

Statistiques

Nombre de vues

109 (dont 2 ULiège)

Nombre de téléchargements

63 (dont 2 ULiège)

Voir plus de statistiques

citations Scopus^®

citations Scopus^®
sans auto-citations

OpenCitations

citations OpenAlex

Bibliographie

Sionkowska, A. Current research on the blends of natural and synthetic polymers as new biomaterials: Review. Prog. Polym. Sci. 2011, 36, 1254-1276.
Felfel, R.M.; Gideon-Adeniyi, M.J.; Zakir Hossain, K.M.; Roberts, G.A.F.; Grant, D.M. Structural, mechanical and swelling characteristics of 3D scaffolds from chitosan-agarose blends. Carbohydr. Polym. 2019, 204, 59-67.
Mano, J.F.; Silva, G.A.; Azevedo, H.S.; Malafaya, P.B.; Sousa, R.A.; Silva, S.S.; Reis, R.L. Natural origin biodegradable systems in tissue engineering and regenerative medicine: Present status and some moving trends Journal of the Royal Society. Interface 2007, 4, 999-1030.
Zhu, J.; Marchant, R.E. Design properties of hydrogel tissue-engineering scaffolds. Expert Rev. Med. Dev. 2011, 8, 607-626.
Ragetly, G.R.; Slavik, G.J.; Cunningham, B.T.; Schaeffer, D.J.; Griffon, D.J. Cartilage tissue engineering on fibrous chitosan scaffolds produced by a replica molding technique. J. Biomed. Mater. Res. Part A 2010, 93, 46-55.
Elieh-Ali-Komi, D.; Hamblin, M.R. Chitin and chitosan: Production and application of versatile biomedical nanomaterials. Int. J. Adv. Res. 2016, 4, 411-427.
Sachar, A.; Strom, T.A.; Serrano, M.J.; Benson, M.D.; Opperman, L.A.; Svoboda, K.K.H.; Liu, H. Osteoblasts responses to three-dimensional nanofibrous gelatin scaffolds. J. Biomed. Mater. Res. A 2012, 100, 3029-3041.
Cukierman, E.; Pankov, R.; Yamada, K.M. Cell interactions with three-dimensional matrices. Curr. Opin. Cell Biol. 2002, 14, 633-639.
Suda, T.; Takahashi, N.; Udagawa, N.; Jimi, E.; Gillespie, M.T.; Martin, T.J. Modulation of osteoclast differentiation and function by the new members of the tumor necrosis factor receptor and ligand families. Endocr. Rev. 1999, 20, 345-357.
Nakashima, T.; Hayashi, M.; Fukunaga, T.; Kurata, K.; Oh-Hora, M.; Feng, J.Q.; Bonewald, L.F.; Kodama, T.; Wutz, A.; Wagner, E.F. et al. Evidence for osteocyte regulation of bone homeostasis through RANKL expression. Nat. Med. 2011, 17, 1231-1234.
Jeevithan, E.; Jeya Shakila, R.; Varatharajakumar, A.; Jeyasekaran, G.; Sukumar, D. Physico-functional and mechanical properties of chitosan and calcium salts incorporated fish gelatin scaffolds. Int. J. Biol. Macromol. 2013, 60, 262-267.
Harper, E.J. Bioactive bone cements. Proc. Inst. Mech. Eng. Part H 1998, 212, 113-120.
Heikkila, J.T.; Aho, A.J.; Kangasniemi, I.; Yli-Urpo, A. Polymethylmethacrylate composites: Disturbed bone formation at the surface of bioactive glass and hydroxyapatite. Biomaterials 1996, 17, 1755-1760.
Sogal, A.; Hulbert, S. Mechanical properties of a composite bone cement: Polymethylmethacrylate and hydroxyapatite. Bioceramic 1992, 5, 213-224.
Pramanik, N.; Mishra, D.; Banerjee, I.; Maiti, T.K.; Bhargava, P.; Pramanik, P. Chemical synthesis, characterization, and biocompatibility study of hydroxyapatite/chitosan phosphate nanocomposite for bone tissue engineering applications. Int. J. Biomater. 2009, 2009, 512417.
Kim, H.D.; Lee, E.A.; An, Y.H.; Kim, S.L.; Lee, S.S.; Yu, S.J.; Jung, L.H.; Nam, K.T.; Im, G.S.; Hwang, S.N. Chondroitin sulfate-based biomineralizing surface hydrogels for bone tissue engineering. ACs Appl. Mater. Interfaces 2017, 9, 21639-21650.
Jeevithan, E.; Zhang, J.; Bao, B.; Palaniyandi, K.; Wang, S.; Wenhui, W.; Robinson, J.S. Rheological, biocompatibility and osteogenesis assessment of fish collagen scaffold for bone tissue engineering. Int. J. Biol. Macromol. 2016, 91, 51-59.
Thangavelu, M.; Adithan, A.; Judith, S.; Nam, S.K.; Jong-Hoon, K. Collagen/chitosan porous bone tissue engineering composite scaffold incorporated with ginseng compound K. Carbohydr. Polym. 2016, 152, 566-574.
Xianshuo, C.; Jun, W.; Min, L.; Yong, C.; Yang, C.; Xiaolong, Y. Chitosan-collagen/organomontmorillonite scaffold for bone tissue engineering. Front Mater. Sci. 2015, 9, 405-412.
Zhang, J.; Jeevithan, E.; Bao, B.; Wang, S.; Gao, K.; Zhang, C.; Wu, W. Structural characterization, in-vivo acute systemic toxicity assessment and in-vitro intestinal absorption properties of tilapia (Oreochromis niloticus) skin acid and pepsin solublilized type I collagen. Process Biochem. 2016, 51, 2017-2025.
Jeevithan, E.; Sanchez, C.; de Val, J.E.M.S.; Henrotin, Y.; Wang, S.; Motaung, K.S.C.M.; Guo, R.; wang, C.; Robinson, J.; Regenstein, J.M. et al. Cross-talk between primary osteocytes and bone marrow macrophages for osteoclastogenesis upon collagen treatment. Sci. Rep. 2018, 8, 5318.
Bills, C.E.; Eisenberg, H.; Pallante, S.L. Complexes of organic acids with calcium phosphate: The Von Kossa stain as a clue to the composition of bone mineral. Johns Hopkins Med. J. 1971, 128, 194-207.
Woessner, J. The determination of hydroxyproline in tissue and protein samples containing small proportions of this amino acid. Arch. Biochem. Biophys. 1974, 93, 440-447.
Neuman, R.E.; Logan, M.A. The determination of hydroxyproline. J. Biol. Chem. 1950, 184, 299-306.
Waynforth, H.B.; Flecknell, P.A. Specific Surgical Operations Experimental and Surgical Techniques in the Rat; Academic Press: London, UK, 1992.
Kamalakar, A.; Washam, C.L.; Akel, N.S.; Allen, B.J.; Williams, D.K.; Swain, F.L.; Leitzel, K.; Lipton, A.; Gaddy, D.; Suva, L.J. PTHrP(12-48) modulates the bone marrow microenvironment and suppresses human osteoclast differentiation and lifespan. J. Bone Miner. Res. 2017, 32, 1421-1431.
Ye, S.; Fowler, T.W.; Pavlos, N.J.; Ng, P.Y.; Liang, K.; Feng, Y.; Zheng, M.; Kurten, R.; Manolagas, C.S.; Zhao, H. LIS1 regulates osteoclast formation and function through its interactions with dynein/dynactin and Plekhm1. PLoS ONE 2011, 6, e27285.
Engler, A.J.; Griffin, M.A.; Sen, S.; Bönnemann, C.G.; Sweeney, H.L.; Discher, D.E. Myotubes differentiate optimally on substrates with tissue-like stiffness: Pathological implications for soft or stiff microenvironments. J. Cell Biol. 2004, 13, 877-887.
Engelberg, I.; Kohn, J. Physico-mechanical properties of degradable polymers used in medical applications: A comparative study. Biomaterials 1991, 12, 292-304.
Maitz, M.F. Applications of synthetic polymers in clinical medicine. J. Mater. Sci. 2015, 1, 161-176.
Li, Z.; Ramay, H.R.; Hauch, K.D.; Xiao, D.; Zhang, M. Chitosan-alginate hybrid scaffolds for bone tissue engineering. Biomaterials 2005, 26, 3919-3928.
Yang, X.J.; Liang, C.Y.; Cai, Y.L.; Hu, K.; Wei, Q.; Cui, Z.D. Recombinant human-like collagen modulated the growth of nano-hydroxyapatite on NiTi alloy. Mater. Sci. Eng. C 2009, 29, 25-28.
Damien, E.; Hing, K.; Saeed, S.; Revell, P.A. A preliminary study on the enhancement of the osteointegration of a novel synthetic hydroxyapatite scaffold in vivo. J. Biomed. Mater. Res. A 2003, 66, 241-246.
Dong, J.; Kojima, H.; Uemura, T.; Kikuchi, M.; Tateishi, T.; Tanaka, J. In vivo evaluation of a novel porous hydroxyapatite to sustain osteogenesis of transplanted bone marrow-derived osteoblastic cells. J. Biomed. Mater. Res. 2001, 57, 208-216.
Loh, Q.L.; Choong, C. Three-Dimensional scaffolds for tissue engineering applications: Role of porosity and pore size. Tissue Eng. Part B Rev. 2013, 19, 485-502.
Jeya Shakila, R.; Jeevithan, E.; Varatharajakumar, A.; Jeyasekaran, G.; Sukumar, D. Comparison of the properties of multi-composite fish gelatin films with that of mammalian gelatin films. Food Chem. 2012, 135, 2260-2267.
Chen, Z.; Mo, X.; He, C.; Wang, H. Intermolecular interactions in electrospun collagen-chitosan complex nanofibers. Carbohydr. Polym. 2008, 72, 410-418.
Azhar, F.F.; Olad, A.; Salehi, R. Fabrication and characterization of chitosan-gelatin/nanohydroxyapatite-polyaniline composite with potential application in tissue engineering scaffolds. Des. Monomer. Polym. 2014, 17, 654-667.
Kim, C.L.; Kim, D.E. Self-healing characteristics of collagen coatings with respect to surface abrasion. Sci. Rep. 2016, 6, 20563.
Bellows, C.G.; Aubin, J.E.; Heersche, J.N. Initiation and progression of mineralization of bone nodules formed in vitro: The role of alkaline phosphatase and organic phosphate. Bone Miner. 1991, 14, 27-40.
Ricchrdo, A.A.; Muzzarelli, F.G.; Alberto, B.; Vincenzo, S.; Antonio, G. Chitosan, hyaluronan and chondroitin sulfate in tissue engineering for cartilage regeneration: A review. Carbohydr. Polym. 2012, 89, 723-739.
Chiu, L.H.; Lai, W.F.; Chang, S.F.; Wong, C.C.; Fan, C.Y.; Fang, C.L.; Tsai, Y.H. The effect of type II collagen on MSC osteogenic differentiation and bone defect repair. Biomaterials 2014, 35, 2680-2691.
Jeevithan, E.; Jung, W.L.; Shujun, W.; Yves, H.; José, E.M.S.V.; Joe, M.R.; Lim, S.Y.; Bao, B.; Wu, W. Evaluation of differentiated bone cells proliferation by blue shark skin collagen via biochemical for bone tissue engineering. Mar. Drug. 2018, 16, 350.
Florencio-Silva, R.; Sasso, G.R.S.; Sasso-Cerri, E.; Simões, M.J.; Cerri, P.S. Biology of bone tissue: Structure, function, and factors that influence bone cells. Biomed. Res. Int. 2015, 2015, 421746.
Guillermin, F.; Beaupied, H.; Fabien-Soulé, V.; Tomé, D.; Benhamou, C.L.; Roux, C.; Blais, A. Hydrolyzed collagen improves bone metabolism and biomechanical parameters in ovariectomized mice: An in vitro and in vivo study. Bone 2010, 46, 827-834.