Advantages and prospects of cell derived decellularized extracellular matrix as tissue engineering scaffolds_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

DU Zhipo ¹ , LIAO Jie ² ^Δ , WANG Bingbing ² ,  YU Suxiang ³ ,  LI Xiaoming ²

1. Department of Orthopedics, the Fourth Central Hospital of Baoding City, Baoding Hebei, 072350, P. R. China;
2. Key Laboratory for Biomechanics and Mechanobiology of Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100083, P. R. China;
3. Department of Pathology, the Fourth Central Hospital of Baoding City, Baoding Hebei, 072350, P. R. China;

Corresponding author：

YU Suxiang, Email: 1197831790@qq.com; LI Xiaoming, Email: x.m.li@hotmail.com

Keywords：

Cell derived decellularized extracellular matrix; tissue engineering scaffold; tissue repair

DOI：

10.7507/1002-1892.202404114

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To review the application of cell derived decellularized extracellular matrix (CDM) in tissue engineering. Methods The literature related to the application of CDM in tissue engineering was extensively reviewed and analyzed. Results CDM is a mixture of cells and their secretory products obtained by culturing cells in vitro for a period of time, and then the mixture is treated by decellularization. Compared with tissue derived decellularized extracellular matrix (TDM), CDM can screen and utilize pathogen-free autologous cells, effectively avoiding the possible shortcomings of TDM, such as immune response and limited sources. In addition, by selecting the cell source, controlling the culture conditions, and selecting the template scaffold, the composition, structure, and mechanical properties of the scaffold can be controlled to obtain the desired scaffold. CDM retains the components and microstructure of extracellular matrix and has excellent biological functions, so it has become the focus of tissue engineering scaffolds. Conclusion CDM is superior in the field of tissue engineering because of its outstanding adjustability, safety, and high bioactivity. With the continuous progress of technology, CDM stents suitable for clinical use are expected to continue to emerge.

Citation： DU Zhipo, LIAO Jie, WANG Bingbing, YU Suxiang, LI Xiaoming. Advantages and prospects of cell derived decellularized extracellular matrix as tissue engineering scaffolds. Chinese Journal of Reparative and Reconstructive Surgery, 2024, 38(11): 1291-1298. doi: 10.7507/1002-1892.202404114 Copy

1.	Gurtner GC, Callaghan MJ, Longaker MT. Progress and potential for regenerative medicine. Annu Rev Med, 2007, 58: 299-312.
2.	Place ES, Evans ND, Stevens MM. Complexity in biomaterials for tissue engineering. Nat Mater, 2009, 8(6): 457-470.
3.	Langer R, Vacanti JP. Tissue engineering. Science, 1993, 260(5110): 920-926.
4.	Feinberg AW. Engineered tissue grafts: opportunities and challenges in regenerative medicine. Wiley Interdiscip Rev Syst Biol Med, 2012, 4(2): 207-220.
5.	Hollister SJ. Porous scaffold design for tissue engineering. Nat Mater, 2005, 4(7): 518-524.
6.	Dutta RC, Dutta AK. Cell-interactive 3D-scaffold; advances and applications. Biotechnol Adv, 2009, 27(4): 334-339.
7.	Kretlow JD, Young S, Klouda L, et al. Injectable biomaterials for regenerating complex craniofacial tissues. Adv Mater, 2009, 21(32-33): 3368-3393.
8.	Franz S, Rammelt S, Scharnweber D, et al. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials, 2011, 32(28): 6692-6709.
9.	Tabata Y. Biomaterial technology for tissue engineering applications. J R Soc Interface, 2009, 6 Suppl 3(Suppl 3): S311-S324.
10.	Chen FM, Zhang J, Zhang M, et al. A review on endogenous regenerative technology in periodontal regenerative medicine. Biomaterials, 2010, 31(31): 7892-7927.
11.	Chen FM, Zhang M, Wu ZF. Toward delivery of multiple growth factors in tissue engineering. Biomaterials, 2010, 31(24): 6279-6308.
12.	Chen FM, An Y, Zhang R, et al. New insights into and novel applications of release technology for periodontal reconstructive therapies. J Control Release, 2011, 149(2): 92-110.
13.	Chen FM, Sun HH, Lu H, et al. Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials, 2012, 33(27): 6320-6344.
14.	Mammoto T, Ingber DE. Mechanical control of tissue and organ development. Development, 2010, 137(9): 1407-1420.
15.	Golebiowska AA, Intravaia JT, Sathe VM, et al. Decellularized extracellular matrix biomaterials for regenerative therapies: Advances, challenges and clinical prospects. Bioact Mater, 2023, 32: 98-123.
16.	Liao J, Xu B, Zhang R, et al. Applications of decellularized materials in tissue engineering: advantages, drawbacks and current improvements, and future perspectives. J Mater Chem B, 2020, 8(44): 10023-10049.
17.	Liao J, Li X, He W, et al. A biomimetic triple-layered biocomposite with effective multifunction for dura repair. Acta Biomater, 2021, 130: 248-267.
18.	Wolchok JC, Tresco PA. The isolation of cell derived extracellular matrix constructs using sacrificial open-cell foams. Biomaterials, 2010, 31(36): 9595-9603.
19.	Hoshiba T, Lu H, Kawazoe N, et al. Decellularized matrices for tissue engineering. Expert Opin Biol Ther, 2010, 10(12): 1717-1728.
20.	Choi YC, Choi JS, Woo CH, et al. Stem cell delivery systems inspired by tissue-specific niches. J Control Release, 2014, 193: 42-50.
21.	Park J, Kim J, Sullivan KM, et al. Decellularized matrix produced by mesenchymal stem cells modulates growth and metabolic activity of hepatic cell cluster. ACS Biomater Sci Eng, 2018, 4(2): 456-462.
22.	Escobedo-Lucea C, Ayuso-Sacido A, Xiong C, et al. Development of a human extracellular matrix for applications related with stem cells and tissue engineering. Stem Cell Rev Rep, 2012, 8(1): 170-183.
23.	Hussey GS, Dziki JL, Badylak SF. Extracellular matrix-based materials for regenerative medicine. Nature Reviews Materials, 2018, 3: 159-173.
24.	Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials, 2011, 32(12): 3233-3243.
25.	Zimmermann R, Nitschke M, Magno V, et al. Discriminant principal component analysis of ToF-SIMS spectra for deciphering compositional differences of MSC-secreted extracellular matrices. Small Methods, 2023, 7(6): e2201157. doi: 10.1002/smtd.202201157.
26.	Chan WW, Yu F, Le QB, et al. Towards biomanufacturing of cell-derived matrices. Int J Mol Sci, 2021, 22(21): 11929. doi: 10.3390/ijms222111929.
27.	Zhang Z, Qu R, Fan T, et al. Stepwise adipogenesis of decellularized cellular extracellular matrix regulates adipose tissue-derived stem cell migration and differentiation. Stem Cells Int, 2019, 2019: 1845926. doi: 10.1155/2019/1845926.
28.	Gilkes DM, Bajpai S, Chaturvedi P, et al. Hypoxia-inducible factor 1 (HIF-1) promotes extracellular matrix remodeling under hypoxic conditions by inducing P4HA1, P4HA2, and PLOD2 expression in fibroblasts. J Biol Chem, 2013, 288(15): 10819-10829.
29.	Eisenberg JL, Safi A, Wei X, et al. Substrate stiffness regulates extracellular matrix deposition by alveolar epithelial cells. Res Rep Biol, 2011, 2011(2): 1-12.
30.	Yang L, Ge L, van Rijn P. Synergistic effect of cell-derived extracellular matrices and topography on osteogenesis of mesenchymal stem cells. ACS Appl Mater Interfaces, 2020, 12(23): 25591-25603.
31.	Lu H, Hoshiba T, Kawazoe N, et al. Autologous extracellular matrix scaffolds for tissue engineering. Biomaterials, 2011, 32(10): 2489-2499.
32.	Gao CY, Huang ZH, Jing W, et al. Directing osteogenic differentiation of BMSCs by cell-secreted decellularized extracellular matrixes from different cell types. J Mater Chem B, 2018, 6(45): 7471-7485.
33.	Marinkovic M, Block TJ, Rakian R, et al. One size does not fit all: developing a cell-specific niche for in vitro study of cell behavior. Matrix Biol, 2016, 52-54: 426-441.
34.	Yao X, Ning LJ, He SK, et al. Stem cell extracellular matrix-modified decellularized tendon slices facilitate the migration of bone marrow mesenchymal stem cells. ACS Biomater Sci Eng, 2019, 5(9): 4485-4495.
35.	Costa-Almeida R, Granja PL, Soares R, et al. Cellular strategies to promote vascularisation in tissue engineering applications. Eur Cell Mater, 2014, 28: 58-67.
36.	Carvalho MS, Silva JC, Cabral JMS, et al. Cultured cell-derived extracellular matrices to enhance the osteogenic differentiation and angiogenic properties of human mesenchymal stem/stromal cells. J Tissue Eng Regen Med, 2019, 13(9): 1544-1558.
37.	D’Amour KA, Bang AG, Eliazer S, et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol, 2006, 24(11): 1392-1401.
38.	Prewitz MC, Seib FP, von Bonin M, et al. Tightly anchored tissue-mimetic matrices as instructive stem cell microenvironments. Nat Methods, 2013, 10(8): 788-794.
39.	Sart S, Yan Y, Li Y, et al. Crosslinking of extracellular matrix scaffolds derived from pluripotent stem cell aggregates modulates neural differentiation. Acta Biomater, 2016, 30: 222-232.
40.	Hoch AI, Mittal V, Mitra D, et al. Cell-secreted matrices perpetuate the bone-forming phenotype of differentiated mesenchymal stem cells. Biomaterials, 2016, 74: 178-187.
41.	Pei M, He F. Extracellular matrix deposited by synovium-derived stem cells delays replicative senescent chondrocyte dedifferentiation and enhances redifferentiation. J Cell Physiol, 2012, 227(5): 2163-2174.
42.	Nyambat B, Manga YB, Chen CH, et al. New insight into natural extracellular matrix: Genipin cross-linked adipose-derived stem cell extracellular matrix gel for tissue engineering. Int J Mol Sci, 2020, 21(14): 4864. doi: 10.3390/ijms21144864.
43.	Zhang X, Li H, Sun J, et al. Cell-derived micro-environment helps dental pulp stem cells promote dental pulp regeneration. Cell Prolif, 2017, 50(5): e12361. doi: 10.1111/cpr.12361.
44.	Zhang W, Yang J, Zhu Y, et al. Extracellular matrix derived by human umbilical cord-deposited mesenchymal stem cells accelerates chondrocyte proliferation and differentiation potential in vitro. Cell Tissue Bank, 2019, 20(3): 351-365.
45.	He SK, Ning LJ, Yao X, et al. Hierarchically demineralized cortical bone combined with stem cell-derived extracellular matrix for regeneration of the tendon-bone interface. Am J Sports Med, 2021, 49(5): 1323-1332.
46.	Si Z, Wang X, Sun C, et al. Adipose-derived stem cells: Sources, potency, and implications for regenerative therapies. Biomed Pharmacother, 2019, 114: 108765. doi: 10.1016/j.biopha.2019.108765.
47.	Nakamura N, Kimura T, Kishida A. Overview of the development, applications, and future perspectives of decellularized tissues and organs. ACS Biomater Sci Eng, 2017, 3(7): 1236-1244.
48.	Kern S, Eichler H, Stoeve J, et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells, 2006, 24(5): 1294-1301.
49.	Chiang CE, Fang YQ, Ho CT, et al. Bioactive decellularized extracellular matrix derived from 3D stem cell spheroids under macromolecular crowding serves as a scaffold for tissue engineering. Adv Healthc Mater, 2021, 10(11): e2100024. doi: 10.1002/adhm.202100024.
50.	Hoshiba T, Yokoyama N. Decellularized extracellular matrices derived from cultured cells at stepwise myogenic stages for the regulation of myotube formation. Biochim Biophys Acta Mol Cell Res, 2020, 1867(4): 118658. doi: 10.1016/j.bbamcr.2020.118658.
51.	Li J, Narayanan K, Zhang Y, et al. Role of lineage-specific matrix in stem cell chondrogenesis. Biomaterials, 2020, 231: 119681. doi: 10.1016/j.biomaterials.2019.119681.
52.	Tang KC, Yang KC, Lin CW, et al. Human adipose-derived stem cell secreted extracellular matrix incorporated into electrospun poly (lactic-co-glycolic acid) nanofibrous dressing for enhancing wound healing. Polymers (Basel), 2019, 11(10): 1609. doi: 10.3390/polym11101609.
53.	Farag A, Vaquette C, Theodoropoulos C, et al. Decellularized periodontal ligament cell sheets with recellularization potential. J Dent Res, 2014, 93(12): 1313-1319.
54.	Kim BS, Choi JS, Kim JD, et al. Recellularization of decellularized human adipose-tissue-derived extracellular matrix sheets with other human cell types. Cell Tissue Res, 2012, 348(3): 559-567.
55.	Santos MS, Cordeiro R, Moura CS, et al. Bioactive nanofibrous scaffolds incorporating decellularized cell-derived extracellular matrix for periodontal tissue engineering. ACS Applied Nano Materials, 2024, 7(4): 4501-4517.
56.	Gu Y, Zhu J, Xue C, et al. Chitosan/silk fibroin-based, Schwann cell-derived extracellular matrix-modified scaffolds for bridging rat sciatic nerve gaps. Biomaterials, 2014, 35(7): 2253-2263.
57.	Aldemir Dikici B, Reilly GC, Claeyssens F. Boosting the osteogenic and angiogenic performance of multiscale porous polycaprolactone scaffolds by in vitro generated extracellular matrix decoration. ACS Appl Mater Interfaces, 2020, 12(11): 12510-12524.
58.	Pati F, Song TH, Rijal G, et al. Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials, 2015, 37: 230-241.
59.	Stanton MM, Parrillo A, Thomas GM, et al. Fibroblast extracellular matrix and adhesion on microtextured polydimethylsiloxane scaffolds. J Biomed Mater Res B Appl Biomater, 2015, 103(4): 861-869.
60.	Xing Q, Vogt C, Leong KW, et al. Highly aligned nanofibrous scaffold derived from decellularized human fibroblasts. Adv Funct Mater, 2014, 24(20): 3027-3035.
61.	Hoshiba T. Cultured cell-derived decellularized extracellular matrix (cultured cell-derived dECM): Future applications and problems—a mini review. Current Opinion in Biomedical Engineering, 2021, 17: 100256. doi: 10.1016/j.cobme.2020.100256.
62.	Murad S, Tajima S, Johnson GR, et al. Collagen synthesis in cultured human skin fibroblasts: effect of ascorbic acid and its analogs. J Invest Dermatol, 1983, 81(2): 158-162.
63.	Han S, Li YY, Chan BP. Extracellular protease inhibition alters the phenotype of chondrogenically differentiating human mesenchymal stem cells (MSCs) in 3D collagen microspheres. PLoS One, 2016, 11(1): e0146928. doi: 10.1371/journal.pone.0146928.
64.	Assunção M, Wong CW, Richardson JJ, et al. Macromolecular dextran sulfate facilitates extracellular matrix deposition by electrostatic interaction independent from a macromolecular crowding effect. Mater Sci Eng C Mater Biol Appl, 2020, 106: 110280. doi: 10.1016/j.msec.2019.110280.
65.	Ang XM, Lee MH, Blocki A, et al. Macromolecular crowding amplifies adipogenesis of human bone marrow-derived mesenchymal stem cells by enhancing the pro-adipogenic microenvironment. Tissue Eng Part A, 2014, 20(5-6): 966-981.
66.	Zeiger AS, Loe FC, Li R, et al. Macromolecular crowding directs extracellular matrix organization and mesenchymal stem cell behavior. PLoS One, 2012, 7(5): e37904. doi: 10.1371/journal.pone.0037904.

1. Gurtner GC, Callaghan MJ, Longaker MT. Progress and potential for regenerative medicine. Annu Rev Med, 2007, 58: 299-312.
2. Place ES, Evans ND, Stevens MM. Complexity in biomaterials for tissue engineering. Nat Mater, 2009, 8(6): 457-470.
3. Langer R, Vacanti JP. Tissue engineering. Science, 1993, 260(5110): 920-926.
4. Feinberg AW. Engineered tissue grafts: opportunities and challenges in regenerative medicine. Wiley Interdiscip Rev Syst Biol Med, 2012, 4(2): 207-220.
5. Hollister SJ. Porous scaffold design for tissue engineering. Nat Mater, 2005, 4(7): 518-524.
6. Dutta RC, Dutta AK. Cell-interactive 3D-scaffold; advances and applications. Biotechnol Adv, 2009, 27(4): 334-339.
7. Kretlow JD, Young S, Klouda L, et al. Injectable biomaterials for regenerating complex craniofacial tissues. Adv Mater, 2009, 21(32-33): 3368-3393.
8. Franz S, Rammelt S, Scharnweber D, et al. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials, 2011, 32(28): 6692-6709.
9. Tabata Y. Biomaterial technology for tissue engineering applications. J R Soc Interface, 2009, 6 Suppl 3(Suppl 3): S311-S324.
10. Chen FM, Zhang J, Zhang M, et al. A review on endogenous regenerative technology in periodontal regenerative medicine. Biomaterials, 2010, 31(31): 7892-7927.
11. Chen FM, Zhang M, Wu ZF. Toward delivery of multiple growth factors in tissue engineering. Biomaterials, 2010, 31(24): 6279-6308.
12. Chen FM, An Y, Zhang R, et al. New insights into and novel applications of release technology for periodontal reconstructive therapies. J Control Release, 2011, 149(2): 92-110.
13. Chen FM, Sun HH, Lu H, et al. Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials, 2012, 33(27): 6320-6344.
14. Mammoto T, Ingber DE. Mechanical control of tissue and organ development. Development, 2010, 137(9): 1407-1420.
15. Golebiowska AA, Intravaia JT, Sathe VM, et al. Decellularized extracellular matrix biomaterials for regenerative therapies: Advances, challenges and clinical prospects. Bioact Mater, 2023, 32: 98-123.
16. Liao J, Xu B, Zhang R, et al. Applications of decellularized materials in tissue engineering: advantages, drawbacks and current improvements, and future perspectives. J Mater Chem B, 2020, 8(44): 10023-10049.
17. Liao J, Li X, He W, et al. A biomimetic triple-layered biocomposite with effective multifunction for dura repair. Acta Biomater, 2021, 130: 248-267.
18. Wolchok JC, Tresco PA. The isolation of cell derived extracellular matrix constructs using sacrificial open-cell foams. Biomaterials, 2010, 31(36): 9595-9603.
19. Hoshiba T, Lu H, Kawazoe N, et al. Decellularized matrices for tissue engineering. Expert Opin Biol Ther, 2010, 10(12): 1717-1728.
20. Choi YC, Choi JS, Woo CH, et al. Stem cell delivery systems inspired by tissue-specific niches. J Control Release, 2014, 193: 42-50.
21. Park J, Kim J, Sullivan KM, et al. Decellularized matrix produced by mesenchymal stem cells modulates growth and metabolic activity of hepatic cell cluster. ACS Biomater Sci Eng, 2018, 4(2): 456-462.
22. Escobedo-Lucea C, Ayuso-Sacido A, Xiong C, et al. Development of a human extracellular matrix for applications related with stem cells and tissue engineering. Stem Cell Rev Rep, 2012, 8(1): 170-183.
23. Hussey GS, Dziki JL, Badylak SF. Extracellular matrix-based materials for regenerative medicine. Nature Reviews Materials, 2018, 3: 159-173.
24. Crapo PM, Gilbert TW, Badylak SF. An overview of tissue and whole organ decellularization processes. Biomaterials, 2011, 32(12): 3233-3243.
25. Zimmermann R, Nitschke M, Magno V, et al. Discriminant principal component analysis of ToF-SIMS spectra for deciphering compositional differences of MSC-secreted extracellular matrices. Small Methods, 2023, 7(6): e2201157. doi: 10.1002/smtd.202201157.
26. Chan WW, Yu F, Le QB, et al. Towards biomanufacturing of cell-derived matrices. Int J Mol Sci, 2021, 22(21): 11929. doi: 10.3390/ijms222111929.
27. Zhang Z, Qu R, Fan T, et al. Stepwise adipogenesis of decellularized cellular extracellular matrix regulates adipose tissue-derived stem cell migration and differentiation. Stem Cells Int, 2019, 2019: 1845926. doi: 10.1155/2019/1845926.
28. Gilkes DM, Bajpai S, Chaturvedi P, et al. Hypoxia-inducible factor 1 (HIF-1) promotes extracellular matrix remodeling under hypoxic conditions by inducing P4HA1, P4HA2, and PLOD2 expression in fibroblasts. J Biol Chem, 2013, 288(15): 10819-10829.
29. Eisenberg JL, Safi A, Wei X, et al. Substrate stiffness regulates extracellular matrix deposition by alveolar epithelial cells. Res Rep Biol, 2011, 2011(2): 1-12.
30. Yang L, Ge L, van Rijn P. Synergistic effect of cell-derived extracellular matrices and topography on osteogenesis of mesenchymal stem cells. ACS Appl Mater Interfaces, 2020, 12(23): 25591-25603.
31. Lu H, Hoshiba T, Kawazoe N, et al. Autologous extracellular matrix scaffolds for tissue engineering. Biomaterials, 2011, 32(10): 2489-2499.
32. Gao CY, Huang ZH, Jing W, et al. Directing osteogenic differentiation of BMSCs by cell-secreted decellularized extracellular matrixes from different cell types. J Mater Chem B, 2018, 6(45): 7471-7485.
33. Marinkovic M, Block TJ, Rakian R, et al. One size does not fit all: developing a cell-specific niche for in vitro study of cell behavior. Matrix Biol, 2016, 52-54: 426-441.
34. Yao X, Ning LJ, He SK, et al. Stem cell extracellular matrix-modified decellularized tendon slices facilitate the migration of bone marrow mesenchymal stem cells. ACS Biomater Sci Eng, 2019, 5(9): 4485-4495.
35. Costa-Almeida R, Granja PL, Soares R, et al. Cellular strategies to promote vascularisation in tissue engineering applications. Eur Cell Mater, 2014, 28: 58-67.
36. Carvalho MS, Silva JC, Cabral JMS, et al. Cultured cell-derived extracellular matrices to enhance the osteogenic differentiation and angiogenic properties of human mesenchymal stem/stromal cells. J Tissue Eng Regen Med, 2019, 13(9): 1544-1558.
37. D’Amour KA, Bang AG, Eliazer S, et al. Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells. Nat Biotechnol, 2006, 24(11): 1392-1401.
38. Prewitz MC, Seib FP, von Bonin M, et al. Tightly anchored tissue-mimetic matrices as instructive stem cell microenvironments. Nat Methods, 2013, 10(8): 788-794.
39. Sart S, Yan Y, Li Y, et al. Crosslinking of extracellular matrix scaffolds derived from pluripotent stem cell aggregates modulates neural differentiation. Acta Biomater, 2016, 30: 222-232.
40. Hoch AI, Mittal V, Mitra D, et al. Cell-secreted matrices perpetuate the bone-forming phenotype of differentiated mesenchymal stem cells. Biomaterials, 2016, 74: 178-187.
41. Pei M, He F. Extracellular matrix deposited by synovium-derived stem cells delays replicative senescent chondrocyte dedifferentiation and enhances redifferentiation. J Cell Physiol, 2012, 227(5): 2163-2174.
42. Nyambat B, Manga YB, Chen CH, et al. New insight into natural extracellular matrix: Genipin cross-linked adipose-derived stem cell extracellular matrix gel for tissue engineering. Int J Mol Sci, 2020, 21(14): 4864. doi: 10.3390/ijms21144864.
43. Zhang X, Li H, Sun J, et al. Cell-derived micro-environment helps dental pulp stem cells promote dental pulp regeneration. Cell Prolif, 2017, 50(5): e12361. doi: 10.1111/cpr.12361.
44. Zhang W, Yang J, Zhu Y, et al. Extracellular matrix derived by human umbilical cord-deposited mesenchymal stem cells accelerates chondrocyte proliferation and differentiation potential in vitro. Cell Tissue Bank, 2019, 20(3): 351-365.
45. He SK, Ning LJ, Yao X, et al. Hierarchically demineralized cortical bone combined with stem cell-derived extracellular matrix for regeneration of the tendon-bone interface. Am J Sports Med, 2021, 49(5): 1323-1332.
46. Si Z, Wang X, Sun C, et al. Adipose-derived stem cells: Sources, potency, and implications for regenerative therapies. Biomed Pharmacother, 2019, 114: 108765. doi: 10.1016/j.biopha.2019.108765.
47. Nakamura N, Kimura T, Kishida A. Overview of the development, applications, and future perspectives of decellularized tissues and organs. ACS Biomater Sci Eng, 2017, 3(7): 1236-1244.
48. Kern S, Eichler H, Stoeve J, et al. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells, 2006, 24(5): 1294-1301.
49. Chiang CE, Fang YQ, Ho CT, et al. Bioactive decellularized extracellular matrix derived from 3D stem cell spheroids under macromolecular crowding serves as a scaffold for tissue engineering. Adv Healthc Mater, 2021, 10(11): e2100024. doi: 10.1002/adhm.202100024.
50. Hoshiba T, Yokoyama N. Decellularized extracellular matrices derived from cultured cells at stepwise myogenic stages for the regulation of myotube formation. Biochim Biophys Acta Mol Cell Res, 2020, 1867(4): 118658. doi: 10.1016/j.bbamcr.2020.118658.
51. Li J, Narayanan K, Zhang Y, et al. Role of lineage-specific matrix in stem cell chondrogenesis. Biomaterials, 2020, 231: 119681. doi: 10.1016/j.biomaterials.2019.119681.
52. Tang KC, Yang KC, Lin CW, et al. Human adipose-derived stem cell secreted extracellular matrix incorporated into electrospun poly (lactic-co-glycolic acid) nanofibrous dressing for enhancing wound healing. Polymers (Basel), 2019, 11(10): 1609. doi: 10.3390/polym11101609.
53. Farag A, Vaquette C, Theodoropoulos C, et al. Decellularized periodontal ligament cell sheets with recellularization potential. J Dent Res, 2014, 93(12): 1313-1319.
54. Kim BS, Choi JS, Kim JD, et al. Recellularization of decellularized human adipose-tissue-derived extracellular matrix sheets with other human cell types. Cell Tissue Res, 2012, 348(3): 559-567.
55. Santos MS, Cordeiro R, Moura CS, et al. Bioactive nanofibrous scaffolds incorporating decellularized cell-derived extracellular matrix for periodontal tissue engineering. ACS Applied Nano Materials, 2024, 7(4): 4501-4517.
56. Gu Y, Zhu J, Xue C, et al. Chitosan/silk fibroin-based, Schwann cell-derived extracellular matrix-modified scaffolds for bridging rat sciatic nerve gaps. Biomaterials, 2014, 35(7): 2253-2263.
57. Aldemir Dikici B, Reilly GC, Claeyssens F. Boosting the osteogenic and angiogenic performance of multiscale porous polycaprolactone scaffolds by in vitro generated extracellular matrix decoration. ACS Appl Mater Interfaces, 2020, 12(11): 12510-12524.
58. Pati F, Song TH, Rijal G, et al. Ornamenting 3D printed scaffolds with cell-laid extracellular matrix for bone tissue regeneration. Biomaterials, 2015, 37: 230-241.
59. Stanton MM, Parrillo A, Thomas GM, et al. Fibroblast extracellular matrix and adhesion on microtextured polydimethylsiloxane scaffolds. J Biomed Mater Res B Appl Biomater, 2015, 103(4): 861-869.
60. Xing Q, Vogt C, Leong KW, et al. Highly aligned nanofibrous scaffold derived from decellularized human fibroblasts. Adv Funct Mater, 2014, 24(20): 3027-3035.
61. Hoshiba T. Cultured cell-derived decellularized extracellular matrix (cultured cell-derived dECM): Future applications and problems—a mini review. Current Opinion in Biomedical Engineering, 2021, 17: 100256. doi: 10.1016/j.cobme.2020.100256.
62. Murad S, Tajima S, Johnson GR, et al. Collagen synthesis in cultured human skin fibroblasts: effect of ascorbic acid and its analogs. J Invest Dermatol, 1983, 81(2): 158-162.
63. Han S, Li YY, Chan BP. Extracellular protease inhibition alters the phenotype of chondrogenically differentiating human mesenchymal stem cells (MSCs) in 3D collagen microspheres. PLoS One, 2016, 11(1): e0146928. doi: 10.1371/journal.pone.0146928.
64. Assunção M, Wong CW, Richardson JJ, et al. Macromolecular dextran sulfate facilitates extracellular matrix deposition by electrostatic interaction independent from a macromolecular crowding effect. Mater Sci Eng C Mater Biol Appl, 2020, 106: 110280. doi: 10.1016/j.msec.2019.110280.
65. Ang XM, Lee MH, Blocki A, et al. Macromolecular crowding amplifies adipogenesis of human bone marrow-derived mesenchymal stem cells by enhancing the pro-adipogenic microenvironment. Tissue Eng Part A, 2014, 20(5-6): 966-981.
66. Zeiger AS, Loe FC, Li R, et al. Macromolecular crowding directs extracellular matrix organization and mesenchymal stem cell behavior. PLoS One, 2012, 7(5): e37904. doi: 10.1371/journal.pone.0037904.

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