Stepwise Proliferation and Chondrogenic Differentiation of Mesenchymal Stem Cells in Collagen Sponges Under Different Microenvironments

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2022 Jun 24

PMID 35742851

Authors

Jing Zheng

Yan Xie

Toru Yoshitomi

Naoki Kawazoe

Yingnan Yang

Guoping Chen

Affiliations

Soon will be listed here.

Abstract

Biomimetic microenvironments are important for controlling stem cell functions. In this study, different microenvironmental conditions were investigated for the stepwise control of proliferation and chondrogenic differentiation of human bone-marrow-derived mesenchymal stem cells (hMSCs). The hMSCs were first cultured in collagen porous sponges and then embedded with or without collagen hydrogels for continual culture under different culture conditions. The different influences of collagen sponges, collagen hydrogels, and induction factors were investigated. The collagen sponges were beneficial for cell proliferation. The collagen sponges also promoted chondrogenic differentiation during culture in chondrogenic medium, which was superior to the effect of collagen sponges embedded with hydrogels without loading of induction factors. However, collagen sponges embedded with collagen hydrogels and loaded with induction factors had the same level of promotive effect on chondrogenic differentiation as collagen sponges during in vitro culture in chondrogenic medium and showed the highest promotive effect during in vivo subcutaneous implantation. The combination of collagen sponges with collagen hydrogels and induction factors could provide a platform for cell proliferation at an early stage and subsequent chondrogenic differentiation at a late stage. The results provide useful information for the chondrogenic differentiation of stem cells and cartilage tissue engineering.

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References

Makris E, Gomoll A, Malizos K, Hu J, Athanasiou K . Repair and tissue engineering techniques for articular cartilage. Nat Rev Rheumatol. 2014; 11(1):21-34. PMC: 4629810. DOI: 10.1038/nrrheum.2014.157. View

Calabrese G, Forte S, Gulino R, Cefali F, Figallo E, Salvatorelli L . Combination of Collagen-Based Scaffold and Bioactive Factors Induces Adipose-Derived Mesenchymal Stem Cells Chondrogenic Differentiation . Front Physiol. 2017; 8:50. PMC: 5288372. DOI: 10.3389/fphys.2017.00050. View

Dong C, Lv Y . Application of Collagen Scaffold in Tissue Engineering: Recent Advances and New Perspectives. Polymers (Basel). 2019; 8(2). PMC: 6432532. DOI: 10.3390/polym8020042. View

Zha K, Sun Z, Yang Y, Chen M, Gao C, Fu L . Recent Developed Strategies for Enhancing Chondrogenic Differentiation of MSC: Impact on MSC-Based Therapy for Cartilage Regeneration. Stem Cells Int. 2021; 2021:8830834. PMC: 8007380. DOI: 10.1155/2021/8830834. View

Redini F, Daireaux M, Mauviel A, Galera P, LOYAU G, Pujol J . Characterization of proteoglycans synthesized by rabbit articular chondrocytes in response to transforming growth factor-beta (TGF-beta). Biochim Biophys Acta. 1991; 1093(2-3):196-206. DOI: 10.1016/0167-4889(91)90123-f. View

Wakitani S, Mitsuoka T, Nakamura N, Toritsuka Y, Nakamura Y, Horibe S . Autologous bone marrow stromal cell transplantation for repair of full-thickness articular cartilage defects in human patellae: two case reports. Cell Transplant. 2004; 13(5):595-600. DOI: 10.3727/000000004783983747. View

Xie Y, Lee K, Wang X, Yoshitomi T, Kawazoe N, Yang Y . Interconnected collagen porous scaffolds prepared with sacrificial PLGA sponge templates for cartilage tissue engineering. J Mater Chem B. 2021; 9(40):8491-8500. DOI: 10.1039/d1tb01559a. View

Aldrich E, Cui X, Murphy C, Lim K, Hooper G, McIlwraith C . Allogeneic mesenchymal stromal cells for cartilage regeneration: A review of in vitro evaluation, clinical experience, and translational opportunities. Stem Cells Transl Med. 2021; 10(11):1500-1515. PMC: 8550704. DOI: 10.1002/sctm.20-0552. View

Higuchi A, Ling Q, Suresh Kumar S, Chang Y, Alarfaj A, Munusamy M . Physical cues of cell culture materials lead the direction of differentiation lineages of pluripotent stem cells. J Mater Chem B. 2020; 3(41):8032-8058. DOI: 10.1039/c5tb01276g. View

10.

Askari M, Bonakdar S, Habibi Anbouhi M, Shahsavarani H, Kargozar S, Khalaj V . Sustained release of TGF-β1 via genetically-modified cells induces the chondrogenic differentiation of mesenchymal stem cells encapsulated in alginate sulfate hydrogels. J Mater Sci Mater Med. 2018; 30(1):7. DOI: 10.1007/s10856-018-6203-9. View

11.

Huang J, Xiong J, Wang D, Zhang J, Yang L, Sun S . 3D Bioprinting of Hydrogels for Cartilage Tissue Engineering. Gels. 2021; 7(3). PMC: 8482067. DOI: 10.3390/gels7030144. View

12.

Canadas R, Pirraco R, Oliveira J, Reis R, Marques A . Stem Cells for Osteochondral Regeneration. Adv Exp Med Biol. 2018; 1059:219-240. DOI: 10.1007/978-3-319-76735-2_10. View

13.

Yang J, Zhang Y, Yue K, Khademhosseini A . Cell-laden hydrogels for osteochondral and cartilage tissue engineering. Acta Biomater. 2017; 57:1-25. PMC: 5545789. DOI: 10.1016/j.actbio.2017.01.036. View

14.

Xie Y, Sutrisno L, Yoshitomi T, Kawazoe N, Yang Y, Chen G . Three-dimensional culture and chondrogenic differentiation of mesenchymal stem cells in interconnected collagen scaffolds. Biomed Mater. 2022; 17(3). DOI: 10.1088/1748-605X/ac61f9. View

15.

Hauptstein J, Forster L, Nadernezhad A, Groll J, Tessmar J, Blunk T . Tethered TGF-β1 in a Hyaluronic Acid-Based Bioink for Bioprinting Cartilaginous Tissues. Int J Mol Sci. 2022; 23(2). PMC: 8781121. DOI: 10.3390/ijms23020924. View

16.

Teng B, Zhang S, Pan J, Zeng Z, Chen Y, Hei Y . A chondrogenesis induction system based on a functionalized hyaluronic acid hydrogel sequentially promoting hMSC proliferation, condensation, differentiation, and matrix deposition. Acta Biomater. 2021; 122:145-159. DOI: 10.1016/j.actbio.2020.12.054. View

17.

Shestovskaya M, Bozhkova S, Sopova J, Khotin M, Bozhokin M . Methods of Modification of Mesenchymal Stem Cells and Conditions of Their Culturing for Hyaline Cartilage Tissue Engineering. Biomedicines. 2021; 9(11). PMC: 8615732. DOI: 10.3390/biomedicines9111666. View

18.

Wu M, Chen G, Li Y . TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res. 2016; 4:16009. PMC: 4985055. DOI: 10.1038/boneres.2016.9. View

19.

Bao W, Li M, Yang Y, Wan Y, Wang X, Bi N . Advancements and Frontiers in the High Performance of Natural Hydrogels for Cartilage Tissue Engineering. Front Chem. 2020; 8:53. PMC: 7028759. DOI: 10.3389/fchem.2020.00053. View

20.

Tang X, Muhammad H, McLean C, Miotla-Zarebska J, Fleming J, Didangelos A . Connective tissue growth factor contributes to joint homeostasis and osteoarthritis severity by controlling the matrix sequestration and activation of latent TGFβ. Ann Rheum Dis. 2018; 77(9):1372-1380. PMC: 6104679. DOI: 10.1136/annrheumdis-2018-212964. View