journal article·2022-09-30Open access

Periosteum-inspired in situ CaP generated nanocomposite hydrogels with strong bone adhesion and superior stretchability for accelerated distraction osteogenesis

Tengfei Lou, Kai Chen, Qiyu Luo, Changsheng Liu, Yuan Yuan, Cunyi Fan

Biomaterials Research· Volume 26· Issue 1

Abstract

Abstract Background Distraction osteogenesis (DO) is an efficacious but lengthy procedure to reconstruct segmental bone defects under the principle of tension-stress, during which the periosteum-mediated mechanical stimulation plays a pivotal role. Inspired by the dynamic process of DO and the mechanical stimulation of periosteum, a new design of bionic periosteum was developed to simulate the mechanical transduction of natural periosteum for the application in DO procedure. Methods In this study, an injectable organic-inorganic hybrid hydrogel was developed based on a novel combination of the PEGylated poly (glycerol sebacate) (PEGS) polymer network and in situ formed CaP nanoparticles (ICPNs). Rat bone marrow mesenchymal stem cells (rBMSCs) and human umbilical vein endothelial cells (HUVECs) were cultured and tested in vitro to evaluate biocompatibility, cell adhesion, proliferation, and pro-osteogenic and pro-angiogenic activity. In vivo experiments were conducted in the rat tibial model of distraction osteogenesis. Results The developed nanocomposite hydrogels exhibited excellent injectability, robust bone adhesion, superior stretchability, and enhanced osteogenic activity. The results of in vitro and in vivo studies showed that PEGS/ICPN hydrogels could promote new bone formation and mineralization during the dynamic distraction process through the synergistic effects of angiogenesis and osteogenesis. Conclusions This periosteum-inspired nanocomposite hydrogel represents a mechanobiology approach for effectively restoring large bone defects through the dynamic DO process.
Source: crossref · Quality: baseline

Research context

OpenAlex topics: Bone Tissue Engineering Materials · Connective tissue disorders research · Bone fractures and treatments

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Orthopaedic Department, Shanghai Sixth People’s Hospital, Shanghai 200233, People’s Republic of China.

Key Laboratory for Ultrafine Materials of Ministry of Education, and School of Materials Science and Engineering, East China University of Science and Technology, Shanghai 200237, People’s Republic of China.

Frontiers Science Center for Materiobiology and Dynamic Chemistry, and Engineering Research Center for Biomedical Materials of Ministry of Education, East China University of Science and Technology, Shanghai 200237, People’s Republic of China.

Funding

the National Natural Science Foundation of China for Innovative Research Groups · the Frontiers Science Center for Materiobiology and Dynamic Chemistry · the National Natural Science Foundation of China · he Key Project of National Natural Science Foundation of China · the National key R&D Program of China

References (54)

Show source-provided references
1. 10.1016/j.bjps.2015.11.00310.1016/j.bjps.2015.11.003 ↗
2. 10.1016/j.jot.2022.01.00210.1016/j.jot.2022.01.002 ↗
3. Ilizarov GA. The tension-stress effect on the genesis and growth of tissues. Part I. the influence of stability of fixation and soft-tissue preservation. Clin Orthop Relat Res. 2014;238(238):249–281.
4. 10.1302/0301-620X.70B4.340359510.1302/0301-620X.70B4.3403595 ↗
5. 10.1002/adhm.20210021510.1002/adhm.202100215 ↗
6. 10.1016/j.biomaterials.2020.12056110.1016/j.biomaterials.2020.120561 ↗
7. 10.1016/j.biomaterials.2020.12053510.1016/j.biomaterials.2020.120535 ↗
8. 10.1039/C1CS15203C10.1039/C1CS15203C ↗
9. Bal-Ozturk A Cecen B Avci-Adali M Topkaya SN Alarcin E Yasayan G et al. Tissue adhesives: from research to clinical translation. Nano Today. 2021;36:101049.10.1016/j.nantod.2020.101049 ↗
10. 10.1021/acs.chemrev.0c0117710.1021/acs.chemrev.0c01177 ↗
11. 10.1038/nmat446310.1038/nmat4463 ↗
12. 10.1002/adma.20200766310.1002/adma.202007663 ↗
13. 10.1126/science.aah636210.1126/science.aah6362 ↗
14. 10.1038/s41586-019-1710-510.1038/s41586-019-1710-5 ↗
15. Tang J Xi K Chen H Wang L Li D Xu Y et al. Flexible osteogenic glue as an all-in-one solution to assist fracture fixation and healing. Adv Funct Mater. 2021;31(38):2102465.10.1002/adfm.202102465 ↗
16. 10.1002/adfm.20210968710.1002/adfm.202109687 ↗
17. 10.1021/acsami.9b0317310.1021/acsami.9b03173 ↗
18. Kuang L Huang J Liu Y Li X Yuan Y Liu C. Injectable hydrogel with NIR light-responsive dual-mode PTH release for osteoregeneration in osteoporosis. Adv Funct Mater. 2021;31(47):2105383.10.1002/adfm.202105383 ↗
19. Xu B Zheng PB Gao F Wang W Zhang HT Zhang XR et al. A mineralized high strength and tough hydrogel for skull bone regeneration. Adv Funct Mater. 2017;27(4):1604327.10.1002/adfm.201604327 ↗
20. Swift J Ivanovska IL Buxboim A Harada T Dingal P Pinter J et al. Nuclear Lamin-a scales with tissue stiffness and enhances matrix-directed differentiation. Science. 341(6149):1240104.10.1126/science.1240104 ↗
21. 10.1186/s13287-016-0392-210.1186/s13287-016-0392-2 ↗
22. Cui C Wu T Gao F Fan C Xu Z Wang H et al. An autolytic high strength instant adhesive hydrogel for emergency self-rescue. Adv Funct Mater. 2018;28(42):1804925.10.1002/adfm.201804925 ↗
23. 10.1021/acsami.8b0108210.1021/acsami.8b01082 ↗
24. Gao Y Han X Chen J Pan Y Yang M Lu L et al. Hydrogel-mesh composite for wound closure. Proc Natl Acad Sci U S A. 2021;118(28):e2103457118.10.1073/pnas.2103457118 ↗
25. Bongio M Lopa S Gilardi M Bersini S Moretti M. A 3D vascularized bone remodeling model combining osteoblasts and osteoclasts in a CaP nanoparticle-enriched matrix. Nanomedicine. 2016;11(9):1073–91.10.2217/nnm-2015-0021 ↗
26. 10.1016/j.yexcr.2004.11.02610.1016/j.yexcr.2004.11.026 ↗
27. Nguyen V Canciani B Cirillo F Anastasia L Peretti GM Mangiavini L. Effect of chemically induced hypoxia on osteogenic and angiogenic differentiation of bone marrow mesenchymal stem cells and human umbilical vein endothelial cells in direct coculture. Cells. 2020;9(3):757.10.3390/cells9030757 ↗
28. Schipani E Ryan HE Didrickson S Kobayashi T Johnson RS. Hypoxia in cartilage: HIF-1α is essential for chondrocyte growth arrest and survival. Genes Dev. 2001;15(21):2865-76.10.1101/gad.934301 ↗
29. Sun L Ma Y Niu H Liu Y Yuan Y Liu C. Recapitulation of in situ endochondral ossification using an injectable hypoxia-mimetic hydrogel. Adv Funct Mater. 2021;31(17):2008515.10.1002/adfm.202101589 ↗
30. 10.1097/00003086-200202000-0000910.1097/00003086-200202000-00009 ↗
31. 10.1016/j.actbio.2012.07.00210.1016/j.actbio.2012.07.002 ↗
32. 10.1016/j.biomaterials.2009.01.02210.1016/j.biomaterials.2009.01.022 ↗
33. 10.1002/adma.20160103010.1002/adma.201601030 ↗
34. 10.1038/nature2139210.1038/nature21392 ↗
35. 10.1002/adfm.20100083810.1002/adfm.201000838 ↗
36. 10.1021/acsami.7b1316710.1021/acsami.7b13167 ↗
37. 10.1002/adma.20200430010.1002/adma.202004300 ↗
38. Krishna L Dhamodaran K Jayadev C Chatterjee K Shetty R Khora SS et al. Nanostructured scaffold as a determinant of stem cell fate. Stem Cell Res Ther. 2016;7(1):188.10.1186/s13287-016-0440-y ↗
39. 10.1038/nmat201310.1038/nmat2013 ↗
40. Lee HP Stowers R Chaudhuri O. Volume expansion and TRPV4 activation regulate stem cell fate in three-dimensional microenvironments. Nat Commun. 2019;10(1):529.10.1038/s41467-019-08465-x ↗
41. 10.1016/j.actbio.2015.02.00310.1016/j.actbio.2015.02.003 ↗
42. 10.1089/ten.tea.2011.012710.1089/ten.tea.2011.0127 ↗
43. 10.1016/j.bone.2003.06.00210.1016/j.bone.2003.06.002 ↗
44. 10.1097/01.blo.0000138186.53426.f910.1097/01.blo.0000138186.53426.f9 ↗
45. 10.1097/PRS.000000000000102410.1097/PRS.0000000000001024 ↗
46. Jia Y Zhu Y Qiu S Xu J Chai Y. Exosomes secreted by endothelial progenitor cells accelerate bone regeneration during distraction osteogenesis by stimulating angiogenesis. Stem Cell Res Ther. 2019;10(1):12.10.1186/s13287-018-1115-7 ↗
47. Khatua C Min S Jung HJ Shin JE Kang H. In situ magnetic control of macroscale nanoligand density regulates the adhesion and differentiation of stem cells. Nano Lett. 2020;20(6):4188-96.10.1021/acs.nanolett.0c00559 ↗
48. 10.1016/S1534-5807(04)00075-910.1016/S1534-5807(04)00075-9 ↗
49. 10.1016/j.biomaterials.2022.12140810.1016/j.biomaterials.2022.121408 ↗
50. 10.1016/j.mattod.2015.01.01910.1016/j.mattod.2015.01.019 ↗
51. Muoz J Akhavan NS Mullins AP Arjmandi BH. Macrophage polarization and osteoporosis: a review. Nutrients. 2020;12(10):2999.10.3390/nu12102999 ↗
52. 10.1002/adma.20200417210.1002/adma.202004172 ↗
53. 10.1007/s12016-020-08824-310.1007/s12016-020-08824-3 ↗
54. 10.1016/j.bioactmat.2022.02.00410.1016/j.bioactmat.2022.02.004 ↗