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Decellularized Extracellular Matrices in Bone Tissue Engineering: From Cells to Tissues. Mini-Review

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An Erratum to this article was published on 01 May 2021

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Abstract

Extracellular matrix (ECM) plays a critical role in the maintenance of cellular survival, proliferation, and differentiation potential. Decellularized ECM (dECM) used in tissue engineering applications mimics the native microenvironment to regulate cellular communications, metabolism, and intracellular signaling pathways relevant to differentiation and tissue regeneration. Herein, we reviewed the sources of dECM utilized in bone tissue engineering and their effects on osteogenesis promotion. PubMed, Science Direct, and Scopus databases were explored to provide original articles published mostly from 2015 to 2020. Then, in vitro and in vivo studies considering advancements on the effect of decellularized extracellular matrices on stem cell osteogenic commitment were reviewed. dECM is mainly extracted from cultures of mesenchymal stem cells (MSCs), fibroblasts, osteoblasts, endothelial cells as well as from bone, periosteum, cartilage, and tendon tissues. dECM provides supportive niches to MSC stemness, proliferation, migration, and osteogenic commitment via triggering substantial intracellular pathways. In general, dECM is discussed as a promising naturally-derived material in bone tissue engineering with the potency to synchronize the cell-substrate interactions, and initiating signaling pathways involved in MSC osteogenic differentiation and tissue reconstruction.

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REFERENCES

  1. Afratis, N.A., Nikitovic, D., Multhaupt, H.A., Theocharis, A.D., Couchman, J.R., and Karamanos, N.K., Syndecans—key regulators of cell signaling and biological functions, The FEBS J., 2017, vol. 284, pp. 27–41.

    CAS  PubMed  Google Scholar 

  2. Alford, A.I., Kozloff, K.M., and Hankenson, K.D., Extracellular matrix networks in bone remodeling, Int. J. Biochem. Cell. Biol., 2015, vol. 65, pp. 20–31.

    CAS  PubMed  Google Scholar 

  3. Alom, N., Peto, H., Kirkham, G.R., Shakesheff, K.M., and White, L.J., Bone extracellular matrix hydrogel enhances osteogenic differentiation of C2C12 myoblasts and mouse primary calvarial cells, J. Biomed. Mater. Res. B. Appl. Biomater., 2018, vol. 106, pp. 900–908.

    CAS  PubMed  Google Scholar 

  4. Bae, S.E., Bhang, S.H., Kim, B.S., and Park, K., Self-assembled extracellular macromolecular matrices and their different osteogenic potential with preosteoblasts and rat bone marrow mesenchymal stromal cells, Biomacromolecules, 2012, vol. 13, pp. 2811–2820.

    CAS  PubMed  Google Scholar 

  5. Baroncelli, M., van der Eerden, B.C., Kan, Y.Y., Alves, R.D., Demmers, J.A., van de Peppel, J., and van Leeuwen, J.P., Comparative proteomic profiling of human osteoblast-derived extracellular matrices identifies proteins involved in mesenchymal stromal cell osteogenic differentiation and mineralization, J. Cell. Physiol., 2018, vol. 233, pp. 387–395.

    CAS  PubMed  Google Scholar 

  6. Beiki, B., Zeynali, B., Taghiabadi, E., Seyedjafari, E., and Kehtari, M., Osteogenic differentiation of Wharton’s jelly-derived mesenchymal stem cells cultured on WJ-scaffold through conventional signalling mechanism, Artif. Cells Nanomed. Biotechnol., 2018, vol. 46, pp. S1032–S1042.

    CAS  PubMed  Google Scholar 

  7. Bryksin, A.V., Brown, A.C., Baksh, M.M., Finn, M., and Barker, T.H., Learning from nature–novel synthetic biology approaches for biomaterial design, Acta Biomaterialia, 2014, vol. 10, pp. 1761–1769.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Burk, J., Plenge, A., Brehm, W., Heller, S., Pfeiffer, B. and Kasper, C., Induction of tenogenic differentiation mediated by extracellular tendon matrix and short-term cyclic stretching, Stem Cells Int., 2016, vol. 2016, article ID  7342379.

  9. Cai, R., Nakamoto, T., Hoshiba, T., Kawazoe, N., and Chen, G., Matrices secreted during simultaneous osteogenesis and adipogenesis of mesenchymal stem cells affect stem cells differentiation, Acta Biomater., 2016, vol. 35, pp. 185–193.

    CAS  PubMed  Google Scholar 

  10. Campana, V., Milano, G., Pagano, E., Barba, M., Cicione, C., Salonna, G., Lattanzi, W., and Logroscino, G., Bone substitutes in orthopaedic surgery: from basic science to clinical practice, J. Mater. Sci. Mater. Med., 2014, vol. 25, pp. 2445–2461.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Carvalho, M.S., Silva, J.C., Cabral, J.M.S., da Silva, C.L. and Vashishth, D., Cultured cell-derived extracellular matrices to enhance the osteogenic differentiation and angiogenic properties of human mesenchymal stem/stromal cells, J. Tissue. Eng. Reg. Med., 2019, vol. 13, pp. 1544–1558.

    CAS  Google Scholar 

  12. Chen, G., Dong, C., Yang, L., and Lv, Y., 3D scaffolds with different stiffness but the same microstructure for bone tissue engineering, ACS Appl. Mater. Inter., 2015, vol. 7, pp. 15790−15802. Chi, H., Chen, G., He, Y., Chen, G., Tu, H., Liu, X., Yan, J., and Wang, X., 3D-HA scaffold functionalized by extracellular matrix of stem cells promotes bone repair, Int. J. Nanomed., 2020, vol. 15, pp. 5825–5838.

    Google Scholar 

  13. Cunniffe, G.M., Díaz-Payno, P.J., Ramey, J.S., Mahon, O.R., Dunne, A., Thompson, E.M., O’Brien, F.J., and Kelly, D.J., Growth plate extracellular matrix-derived scaffolds for large bone defect healing, Eur. Cell. Mater., 2017, vol. 33. pp. 130–142.

    CAS  PubMed  Google Scholar 

  14. Decaris, M.L., Mojadedi, A., Bhat, A., and Leach, J.K., Transferable cell-secreted extracellular matrices enhance osteogenic differentiation, Acta. Biomater., 2012, vol. 8, pp. 744–752.

    CAS  PubMed  Google Scholar 

  15. Deng, M., Luo, K., Hou, T., Luo, F., Xie, Z., Zhang, Z., Yang, A., Yu, B., Yi, S., Tan, J., Dong, S., and Xu, J., IG-FBP3 deposited in the human umbilical cord mesenchymal stem cell-secreted extracellular matrix promotes bone formation, J. Cell. Physiol., 2018, vol. 233, pp. 5792–5804.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Dong, R., Bai, Y., Dai, J., Deng, M., Zhao, C., Tian, Z., Zeng, F., Liang, W., Liu, L., and Dong, S., Engineered scaffolds based on mesenchymal stem cells/preosteoclasts extracellular matrix promote bone regeneration, J. Tissue Eng., 2020, vol. 11, pp. 1–13.

    CAS  Google Scholar 

  17. Fitzpatrick, L.E. and McDevitt, T.C., Cell-derived matrices for tissue engineering and regenerative medicine applications, Biomater. Sci., 2015, vol 3, pp. 12–24.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Frantz, C., Stewart, K.M., and Weaver, V.M., The extracellular matrix at a glance, J. Cell. Sci., 2010, vol. 123, pp. 4195–4200.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Freeman, F.E., Browe, D.C., Nulty, J., Von Euw, S., Grayson, W.L., and Kelly, D.J., Biofabrication of multiscale bone extracellular matrix scaffolds for bone tissue engineering, Eur. Cell. Mater., 2019, vol. 38, pp. 168–187.

    CAS  PubMed  Google Scholar 

  20. Gao, C.Y., Huang, Z.H., Jing, W., Wei, P.F., Jin, L., Zhang, X.H., Cai, Q., Deng, X.L. and Yang, X.P., Directing osteogenic differentiation of BMSCs by cell-secreted decellularized extracellular matrixes from different cell types, J. Mater. Chem. B., 2018, vol. 6, pp. 7471–7485.

    CAS  PubMed  Google Scholar 

  21. Getova, V.E., van Dongen, J.A., Brouwer, L.A., and Harmsen, M.C., Adipose tissue-derived ECM hydrogels and their use as 3D culture scaffold, Artif. Cells Nanomed. Biotechnol., 2019, vol. 47, pp. 1693–1701.

    CAS  PubMed  Google Scholar 

  22. Harvestine, J.N., Orbay, H., Chen, J.Y., Sahar, D.E., and Leach, J.K., Cell-secreted extracellular matrix, independent of cell source, promotes the osteogenic differentiation of human stromal vascular fraction, J. Mater. Chem. B., 2018, vol., pp. 4104–4115.

  23. He, J., Li, Z., Yu, T., Wang, W., Tao, M., Ma, Y., Wang, S., Fan, J., Tian, X., Wang, X., Lin, Y., and Ao, Q., Preparation and evaluation of acellular sheep periostea for guided bone regeneration, J. Biomed. Mater. Res. A., 2020, vol. 108, pp. 19–29.

    CAS  PubMed  Google Scholar 

  24. Heng, B.C., Zhu, S., Xu, J., Yuan, C., Gong, T., and Zhang, C., Effects of decellularized matrices derived from periodontal ligament stem cells and SHED on the adhesion, proliferation and osteogenic differentiation of human dental pulp stem cells in vitro, Tissue Cell, 2016, vol. 48, pp. 133–143.

    CAS  PubMed  Google Scholar 

  25. Hoch, A.I., Mittal, V., Mitra, D., Vollmer, N., Zikry, C.A., and Leach, J.K., Cell-secreted matrices perpetuate the bone-forming phenotype of differentiated mesenchymal stem cells, Biomaterials, 2016, vol. 74, pp. 178–187.

    CAS  PubMed  Google Scholar 

  26. Hoshiba, T. and Tanaka, M., Decellularized matrices as in vitro models of extracellular matrix in tumor tissues at different malignant levels: mechanism of 5-fluorouracil resistance in colorectal tumor cells, Biochim. Biophys. Acta, 2016, vol. 1863, pp. 2749–2757.

    CAS  PubMed  Google Scholar 

  27. Hwang, M.P., Subbiah, R., Kim, I.G., Lee, K.E., Park, J., Kim, S.H., and Park, K., Approximating bone ECM: crosslinking directs individual and coupled osteoblast/osteoclast behavior, Biomaterials, 2016, vol. 103, pp. 22–32.

    CAS  PubMed  Google Scholar 

  28. Junka, R., Quevada, K., and Yu, X., Acellular polycaprolactone scaffolds laden with fibroblast/endothelial cell-derived extracellular matrix for bone regeneration, J. Biomed. Mater. Res. A, 2020, vol. 108, pp. 351–364.

    CAS  PubMed  Google Scholar 

  29. Kang, Y., Kim, S., Bishop, J., Khademhosseini, A., and Yang, Y., The osteogenic differentiation of human bone marrow MSCs on HUVEC-derived ECM and β-TCP scaffold, Biomaterials, 2012, vol. 33, pp. 6998–7007.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kim, B., Ventura, R., and Lee, B.T., Functionalization of porous BCP scaffold by generating cell-derived extracellular matrix from rat bone marrow stem cells culture for bone tissue engineering, J. Tissue Eng. Reg. Med., 2018, vol. 12, pp. e1256–e1267.

    CAS  Google Scholar 

  31. Kim, J. and Ma, T., Autocrine fibroblast growth factor 2-mediated interactions between human mesenchymal stem cells and the extracellular matrix under varying oxygen tension, J. Cell Biochem., 2013, vol. 114, pp. 716–727.

    CAS  PubMed  Google Scholar 

  32. Ko, E., Alberti, K., Lee, J.S., Yang, K., Jin, Y., Shin, J., Yang, H.S., Xu, Q., and Cho, S.-W., Nanostructured tendon-derived scaffolds for enhanced bone regeneration by human adipose-derived stem cells, ACS Appl. Mater. Interfaces, 2016, vol. 8, pp. 22819–22829.

    CAS  PubMed  Google Scholar 

  33. Kolf, C.M., Song, L., Helm, J., and Tuan, R.S., Nascent osteoblast matrix inhibits osteogenesis of human mesenchymal stem cells in vitro, Stem Cell Res. Ther., 2015, vol. 6, article no. 258. https://doi.org/10.1186/s13287-015-0223-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Lee, M.K., Lin, S.P., HuangFu, W.C., Yang, D.S., and Liu, I.H., Endothelial-derived extracellular matrix ameliorate the stemness deprivation during ex vivo expansion of mouse bone marrow- derived mesenchymal stem cells, PLoS One, 2017, vol. 12, e0184111.

    PubMed  PubMed Central  Google Scholar 

  35. Li, M., Chen, X., Yan, J., Zhou, L., Wang, Y., He, F., Lin, J., Zhu, C., Pan, G., Yu, J., Pei, M., Yang, H., and Liu, T., Inhibition of osteoclastogenesis by stem cell-derived extracellular matrix through modulation of intracellular reactive oxygen species, Acta Biomater., 2018, vol. 71, pp. 118–131.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Lin, X., Zhao, C., Zhu, P., Chen, J., Yu, H., Cai, Y., Zhang, Q., Qin, A., and Fan, S., Periosteum extracellular-matrix-mediated acellular mineralization during bone formation, Adv. Healthc. Mater., 2018, vol. 7(4), article no. 1700660. https://doi.org/10.1002/adhm.201700660

    Article  CAS  Google Scholar 

  37. Liu, H., Yang, L., Zhang, E., Zhang, R., Cai, D., Zhu, S., Ran, J., Bunpetch, V., Cai, Y., Heng, B.C., Hu, Y., Dai, X., Chen, X., and Ouyang, H., Biomimetic tendon extracellular matrix composite gradient scaffold enhances ligament-to-bone junction reconstruction, Acta Biomater., 2017, vol. 56, pp. 129–140.

    CAS  PubMed  Google Scholar 

  38. Liu, S., Wang, Y., Wang, J., Qiu, P., Wang, S., Shi, Y., Li, M., Chen, P., Lin, X., and Fang, X., A cancellous bone matrix system with specific mineralisation degrees for mesenchymal stem cell differentiation and bone regeneration, Biomater. Sci., 2019, vol. 7, pp. 2452–2467.

    CAS  PubMed  Google Scholar 

  39. Mao, Y., Hoffman, T., Wu, A., Goyal, R., and Kohn, J., Cell type-specific extracellular matrix guided the differentiation of human mesenchymal stem cells in 3D polymeric scaffolds, J. Mater. Sci. Mater. Med., 2017, vol. 28, article no. 100. https://doi.org/10.1007/s10856-017-5912-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Miron, R.J., Bosshardt, D.D., Zhang, Y., Buser, D., and Sculean, A., Gene array of primary human osteoblasts exposed to enamel matrix derivative in combination with a natural bone mineral, Clin. Oral. Investig., 2013, vol. 17, pp. 405–410.

    PubMed  Google Scholar 

  41. Motoike, S., Kajiya, M., Komatsu, N., Horikoshi, S., Ogawa, T., Sone, H., Matsuda, S., Ouhara, K., Iwata, T., Mizuno, N., Fujita, T., Ikeya, M., and Kurihara, H., Clumps of mesenchymal stem cell/extracellular matrix complexes generated with xeno-free conditions facilitate bone regeneration via direct and indirect osteogenesis, Int. J. Mol. Sci., 2019, vol. 20, article no. 3970. https://doi.org/10.3390/ijms20163970

    Article  CAS  PubMed Central  Google Scholar 

  42. Mountziaris, P.M., Tzouanas, S.N., and Mikos, A.G., The interplay of bone-like extracellular matrix and TNF-α signaling on in vitro osteogenic differentiation of mesenchymal stem cells, J. Biomed. Mater. Res. A, 2012, vol. 100, pp. 1097–1106.

    PubMed  PubMed Central  Google Scholar 

  43. Park, M.H., Subbiah, R., Kwon, M.J., Kim, W.J., Kim, S.H., Park, K. and Lee, K., The three dimensional cues-integrated-biomaterial potentiates differentiation of human mesenchymal stem cells, Carbohydr. Polym., 2018, vol. 202, pp. 488–496.

    CAS  PubMed  Google Scholar 

  44. Qiu, P., Li, M., Chen, K., Fang, B., Chen, P., Tang, Z., Lin, X., and Fan, S., Periosteal matrix- derived hydrogel promotes bone repair through an early immune regulation coupled with enhanced angio- and osteogenesis, Biomaterials, 2020, vol. 227, article no. 119552. https://doi.org/10.1016/j.biomaterials.2019.119552

    Article  CAS  PubMed  Google Scholar 

  45. Senthebane, D.A., Jonker, T., Rowe, A., Thomford, N.E., Munro, D., Dandara, C., Wonkam, A., Govender, D., Calder, B., and Soares, N.C., The role of tumor microenvironment in chemoresistance: 3D extracellular matrices as accomplices, Int J. Mol. Sci., 2018, vol. 19, article no. 2861. https://doi.org/10.3390/ijms19102861

    Article  CAS  PubMed Central  Google Scholar 

  46. Silva, J.C., Carvalho, M.S., Udangawa, R.N., Moura, C.S., Cabral, J.M.S., C, L.d.S., Ferreira, F.C., Vashishth, D., and Linhardt, R.J., Extracellular matrix decorated polycaprolactone scaffolds for improved mesenchymal stem/stromal cell osteogenesis towards a patient-tailored bone tissue engineering approach, J. Biomed. Mater. Res. B., Appl. Biomater., 2020, vol. 108, pp. 2153–2166.

    CAS  Google Scholar 

  47. Simunovic, F., Winninger, O., Strassburg, S., Koch, H.G., Finkenzeller, G., Stark, G.B., and Lampert, F.M., Increased differentiation and production of extracellular matrix components of primary human osteoblasts after cocultivation with endothelial cells: A quantitative proteomics approach, J. Cell. Biochem., 2019, vol. 120, pp. 396–404.

    CAS  PubMed  Google Scholar 

  48. Su, M., Zhang, Q., Zhu, Y., Wang, S., Lv, J., Sun, J., Qiu, P., Fan, S., Jin, K., Chen, L., and Lin, X., Preparation of decellularized triphasic hierarchical bone-fibrocartilage-tendon composite extracellular matrix for enthesis regeneration, Adv. Healthc. Mater., 2019, vol. 8, e1900831. https://doi.org/10.1002/adhm.201900831

    Article  CAS  PubMed  Google Scholar 

  49. Sun, T., Yao, S., Liu, M., Yang, Y., Ji, Y., Cui, W., Qu, Y., and Guo, X., Composite scaffolds of mineralized natural extracellular matrix on true bone ceramic induce bone regeneration through Smad1/5/8 and ERK1/2 pathways, Tissue. Eng. A, 2018, vol. 24, pp. 502–515.

    CAS  Google Scholar 

  50. Sutha, K., Schwartz, Z., Wang, Y., Hyzy, S., Boyan, B.D., and McDevitt, T.C., Osteogenic embryoid body-derived material induces bone formation in vivo, Sci. Rep., 2015, vol. 5, article no. 9960. https://doi.org/10.1038/srep09960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Takagi, K., Fukunaga, S., Nishi, A., Shojima, T., Yoshikawa, K., Hori, H., Akashi, H., and Aoyagi, S., In vivo recellularization of plain decellularized xenografts with specific cell characterization in the systemic circulation: histological and immunohistochemical study, Artif. Organs., 2006, vol. 30, pp. 233–241.

    CAS  PubMed  Google Scholar 

  52. Taylor, D.A., Sampaio, L.C., Ferdous, Z., Gobin, A.S., and Taite, L.J., Decellularized matrices in regenerative medicine, Acta. Biomater., 2018, vol. 74, pp. 74–89.

    CAS  PubMed  Google Scholar 

  53. Theocharis, A.D., Skandalis, S.S., Gialeli, C., and Karamanos, N.K., Extracellular matrix structure, Adv. Drug. Deliv. Rev., 2016, vol. 97, pp. 4–27.

    CAS  PubMed  Google Scholar 

  54. Tour, G., Wendel, M., and Tcacencu, I., Cell-derived matrix enhances osteogenic properties of hydroxyapatite, Tissue. Eng. Part A, 2011, vol. 17, pp. 127−137.

    CAS  PubMed  Google Scholar 

  55. Ventre, M., Coppola, V., Natale, C.F., and Netti, P.A., Aligned fibrous decellularized cell derived matrices for mesenchymal stem cell amplification, J. Biomed. Mater. Res. A., 2019, vol. 107, pp. 2536–2546.

    CAS  PubMed  Google Scholar 

  56. Visser, J., Gawlitta, D., Benders, K.E., Toma, S.M., Pouran, B., van Weeren, P.R., Dhert, W.J., and Malda, J., Endochondral bone formation in gelatin methacrylamide hydrogel with embedded cartilage-derived matrix particles, Biomaterials, 2015, vol. 37, pp. 174–182.

    CAS  PubMed  Google Scholar 

  57. Wang, X., Yu, T., Chen, G., Zou, J., Li, J., and Yan, J., Preparation and characterization of a chitosan/gelatin/extracellular matrix scaffold and its application in tissue engineering, Tissue. Eng. Part C Methods, 2017, vol. 23, pp. 169–179.

    CAS  PubMed  Google Scholar 

  58. Wei, W., Li, J., Chen, S., Chen, M., Xie, Q., Sun, H., Ruan, J., Zhou, H., Bi, X., Zhuang, A., You, Z., Gu, P., and Fan, X., In vitro osteogenic induction of bone marrow mesenchymal stem cells with a decellularized matrix derived from human adipose stem cells and in vivo implantation for bone regeneration, J. Mater. Chem. B, 2017, vol. 5, pp. 2468–2482.

    CAS  PubMed  Google Scholar 

  59. Wen, Y., Yang, H., Wu, J., Wang, A., Chen, X., Hu, S., Zhang, Y., Bai, D., and Jin, Z., COL4A2 in the tissue-specific extracellular matrix plays important role on osteogenic differentiation of periodontal ligament stem cells, Theranostics, 2019, vol 9, pp. 4265–4286.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Wu, R.X., He, X.T., Zhu, J.H., Yin, Y., Li, X., Liu, X., and Chen, F.M., Modulating macrophage responses to promote tissue regeneration by changing the formulation of bone extracellular matrix from filler particles to gel bioscaffolds, Mater. Sci. Eng., C Mater. Biol. Appl., 2019, vol. 101, pp. 330–340.

    CAS  Google Scholar 

  61. Xing, Q., Qian, Z., Kannan, B., Tahtinen, M., and Zhao, F., Osteogenic differentiation evaluation of an engineered extracellular matrix based tissue sheet for potential periosteum replacement, ACS Appl. Mater. Inter., 2015, vol. 7, pp. 23239–23247.

    CAS  Google Scholar 

  62. Yang, L., Ge, L., and van Rijn, P., Synergistic effect of cell-derived extracellular matrices and topography on osteogenesis of mesenchymal stem cells, ACS Appl. Mater. Inter., 2020, vol. 12, pp. 25 591–25 603.

    Google Scholar 

  63. Zhang, C., Li, M., Zhu, J., Luo, F., and Zhao, J., Enhanced bone repair induced by human adipose- derived stem cells on osteogenic extracellular matrix ornamented small intestinal submucosa, Reg. Med., 2017, vol. 12, pp. 541–552.

    Google Scholar 

  64. Zhang, L., Qian, Z., Tahtinen, M., Qi, S., and Zhao, F., Prevascularization of natural nanofibrous extracellular matrix for engineering completely biological three-dimensional prevascularized tissues for diverse applications, J. Tissue. Eng. Reg. Med., 2018, vol. 12, pp. e1325–e1336.

    CAS  Google Scholar 

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Funding

This work was financially supported by Iran University of Medical Sciences (grant no. 97028733186).

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Authors and Affiliations

  1. Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Iran University of Medical Sciences, Tehran, Iran

    Azam Bozorgi Zarrini

  2. Fertility and Infertility Research Center, Health Technology Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran

    Maryam Bozorgi & Mozafar Khazaei

  3. Cellular and Molecular Research Center, Iran University of Medical Sciences, Tehran, Iran

    Mansooreh Soleimani

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Abbreviations: dECM—decellularized extracellular matrix, MSC—mesenchymal stem cell, CDM—cell-derived decellularized ECM, BTE—bone tissue engineering.

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Azam Bozorgi Zarrini, Bozorgi, M., Khazaei, M. et al. Decellularized Extracellular Matrices in Bone Tissue Engineering: From Cells to Tissues. Mini-Review. Cell Tiss. Biol. 14, 399–406 (2020). https://doi.org/10.1134/S1990519X20060127

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