Fabrication of Initial Trabecular Bone-inspired Three-dimensional Structure with Cell Membrane Nano Fragments

Overview

Journal Regen Biomater

Specialty Biomedical Engineering

Date 2023 Jan 23

PMID 36683756

Authors

Koichi Kadoya

Emilio Satoshi Hara

Masahiro Okada

Yu Yang Jiao

Takayoshi Nakano

Akira Sasaki

Takuya Matsumoto

Affiliations

Soon will be listed here.

Abstract

The extracellular matrix of trabecular bone has a large surface exposed to the bone marrow and plays important roles such as hematopoietic stem cell niche formation and maintenance. reproduction of trabecular bone microenvironment would be valuable not only for developing a functional scaffold for bone marrow tissue engineering but also for understanding its biological functions. Herein, we analyzed and reproduced the initial stages of trabecular bone formation in mouse femur epiphysis. We identified that the trabecular bone formation progressed through the following steps: (i) partial rupture of hypertrophic chondrocytes; (ii) calcospherite formation on cell membrane nano fragments (CNFs) derived from the ruptured cells; and (iii) calcospherite growth and fusion to form the initial three-dimensional (3D) structure of trabecular bones. For reproducing the initial trabecular bone formation , we collected CNFs from cultured cells and used as nucleation sites for biomimetic calcospherite formation. Strikingly, almost the same 3D structure of the initial trabecular bone could be obtained by using additional CNFs as a binder to fuse biomimetic calcospherites.

References

Suzuki N, Ohneda O, Minegishi N, Nishikawa M, Ohta T, Takahashi S . Combinatorial Gata2 and Sca1 expression defines hematopoietic stem cells in the bone marrow niche. Proc Natl Acad Sci U S A. 2006; 103(7):2202-7. PMC: 1413708. DOI: 10.1073/pnas.0508928103. View

Zhang X . Interactions between cancer cells and bone microenvironment promote bone metastasis in prostate cancer. Cancer Commun (Lond). 2019; 39(1):76. PMC: 6873445. DOI: 10.1186/s40880-019-0425-1. View

Morrison S, Scadden D . The bone marrow niche for haematopoietic stem cells. Nature. 2014; 505(7483):327-34. PMC: 4514480. DOI: 10.1038/nature12984. View

Curtis K, Mai C, Martin H, Oberman A, Alderfer L, Romero-Moreno R . The effect of marrow secretome and culture environment on the rate of metastatic breast cancer cell migration in two and three dimensions. Mol Biol Cell. 2021; 32(10):1009-1019. PMC: 8101488. DOI: 10.1091/mbc.E19-12-0682. View

Anderson H, Garimella R, Tague S . The role of matrix vesicles in growth plate development and biomineralization. Front Biosci. 2004; 10:822-37. DOI: 10.2741/1576. View

Crane G, Ishaug S, Mikos A . Bone tissue engineering. Nat Med. 1995; 1(12):1322-4. DOI: 10.1038/nm1295-1322. View

Kiuru M, Hidaka C, Hubner R, Solomon J, Krause A, Leopold P . Sonic hedgehog expands diaphyseal trabecular bone altering bone marrow niche and lymphocyte compartment. Mol Ther. 2009; 17(8):1442-52. PMC: 2835226. DOI: 10.1038/mt.2009.102. View

Widmer M, Gupta P, Lu L, Meszlenyi R, EVANS G, Brandt K . Manufacture of porous biodegradable polymer conduits by an extrusion process for guided tissue regeneration. Biomaterials. 1998; 19(21):1945-55. DOI: 10.1016/s0142-9612(98)00099-4. View

Iwamoto M, Ohta Y, Larmour C, Enomoto-Iwamoto M . Toward regeneration of articular cartilage. Birth Defects Res C Embryo Today. 2013; 99(3):192-202. PMC: 4089504. DOI: 10.1002/bdrc.21042. View

10.

Hollister S . Porous scaffold design for tissue engineering. Nat Mater. 2005; 4(7):518-24. DOI: 10.1038/nmat1421. View

11.

Chubb R, Oh J, Riley A, Kimura T, Wu S, Wu J . In Vivo Rescue of the Hematopoietic Niche By Pluripotent Stem Cell Complementation of Defective Osteoblast Compartments. Stem Cells. 2017; 35(10):2150-2159. PMC: 5610643. DOI: 10.1002/stem.2670. View

12.

Calvi L, Adams G, Weibrecht K, Weber J, Olson D, Knight M . Osteoblastic cells regulate the haematopoietic stem cell niche. Nature. 2003; 425(6960):841-6. DOI: 10.1038/nature02040. View

13.

Boanini E, Torricelli P, Gazzano M, Giardino R, Bigi A . Nanocomposites of hydroxyapatite with aspartic acid and glutamic acid and their interaction with osteoblast-like cells. Biomaterials. 2006; 27(25):4428-33. DOI: 10.1016/j.biomaterials.2006.04.019. View

14.

Cheng A, Schwartz Z, Kahn A, Li X, Shao Z, Sun M . Advances in Porous Scaffold Design for Bone and Cartilage Tissue Engineering and Regeneration. Tissue Eng Part B Rev. 2018; 25(1):14-29. PMC: 6388715. DOI: 10.1089/ten.TEB.2018.0119. View

15.

Allocca G, Hughes R, Wang N, Brown H, Ottewell P, Brown N . The bone metastasis niche in breast cancer-potential overlap with the haematopoietic stem cell niche . J Bone Oncol. 2019; 17:100244. PMC: 6582079. DOI: 10.1016/j.jbo.2019.100244. View

16.

Haider M, Smit D, Taipaleenmaki H . The Endosteal Niche in Breast Cancer Bone Metastasis. Front Oncol. 2020; 10:335. PMC: 7082928. DOI: 10.3389/fonc.2020.00335. View

17.

Cyboron G, Wuthier R . Purification and initial characterization of intrinsic membrane-bound alkaline phosphatase from chicken epiphyseal cartilage. J Biol Chem. 1981; 256(14):7262-8. View

18.

Mahadik B, Bharadwaj N, Ewoldt R, Harley B . Regulating dynamic signaling between hematopoietic stem cells and niche cells via a hydrogel matrix. Biomaterials. 2017; 125:54-64. PMC: 5444543. DOI: 10.1016/j.biomaterials.2017.02.013. View

19.

Bertran O, Del Valle L, Revilla-Lopez G, Chaves G, Cardus L, Casas M . Mineralization of DNA into nanoparticles of hydroxyapatite. Dalton Trans. 2013; 43(1):317-27. DOI: 10.1039/c3dt52112e. View

20.

Ono N, Ono W, Mizoguchi T, Nagasawa T, Frenette P, Kronenberg H . Vasculature-associated cells expressing nestin in developing bones encompass early cells in the osteoblast and endothelial lineage. Dev Cell. 2014; 29(3):330-9. PMC: 4083679. DOI: 10.1016/j.devcel.2014.03.014. View