10.1007/s40204-019-0108-7

A silk fibroin/decellularized extract of Wharton’s jelly hydrogel intended for cartilage tissue engineering

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  • Arefeh Basiri1,
  • Mehdi Farokhi2,
  • Mahmoud Azami1,
  • Somayeh Ebrahimi-Barough1,
  • Abdolreza Mohamadnia3,
  • Morteza Rashtbar1,
  • Elham Hasanzadeh1,
  • Narges Mahmoodi4,
  • Mohamadreza Baghaban Eslaminejad5,
  • Jafar Ai*1,
  1. Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, IR
  2. National Cell Bank of Iran, Pasteur Institute of Iran, Tehran, IR
  3. Department of Biotechnology, School of Advanced Technologies in Medicine, Shahid Beheshti University of Medical Sciences, Tehran, IR
  4. Sina Trauma and Surgery Reasearch Center, Tehran University of Medical Sciences, Tehran, IR
  5. Department of Stem Cells and Developmental Biology, Cell Science Research Center, Royan Institute for Stem Cell Biology and Technology, ACECR, Tehran, IR
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Published in Issue 2019-01-31

How to Cite

Basiri, A., Farokhi, M., Azami, M., Ebrahimi-Barough, S., Mohamadnia, A., Rashtbar, M., Hasanzadeh, E., Mahmoodi, N., Baghaban Eslaminejad, M., & Ai, J. (2019). A silk fibroin/decellularized extract of Wharton’s jelly hydrogel intended for cartilage tissue engineering. Progress in Biomaterials, 8(1 (March 2019). https://doi.org/10.1007/s40204-019-0108-7
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Abstract

Abstract A hybrid hydrogel was obtained from decellularized extract from Wharton’s jelly (DEWJ) and silk fibroin (SF) and characterized for cartilage tissue engineering. Wharton’s jelly was used due to its similarity with articular cartilage in extracellular matrix composition. Also, silk fibroin has good mechanical properties which make this construct appropriate for cartilage repair. Decellularization of Wharton’s jelly was verified by DAPI staining, DNA quantification, and PCR analysis. Then, the biochemical composition of DEWJ was determined by ELISA kits for total proteins, collagens, sulfated glycosaminoglycans (sGAG), and transforming growth factor β1 (TGF-β1). After fabricating pure SF and SF/DEWJ hybrid hydrogels, their physical and mechanical properties were characterized by FESEM, Fourier-transform infrared spectroscopy (FTIR) and rheological assays (amplitude and frequency sweeps). Furthermore, cell viability and proliferation were assessed by MTT assay. The results have shown that DEWJ in hybrid hydrogels enhances mechanical properties of the construct relative to pure SF hydrogels. Also, this extract at its 40% concentration in culture media and 20% or 40% concentrations in SF/DEWJ hybrid hydrogels significantly increases population of the cells compared to control and pure SF hydrogel after 7 days. In conclusion, this study proposes the potential of SF/DEWJ hybrid hydrogels for cartilage tissue engineering applications.

Keywords

  • Decellularization,
  • Wharton’s jelly,
  • Silk fibroin,
  • Hydrogel,
  • Cartilage tissue engineering
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References

  1. Ahmadi et al. (2017) Osteogenic differentiation of mesenchymal stem cells cultured on PLLA scaffold coated with Wharton’s Jelly
  2. Arno et al. (2014) Effect of human Wharton’s jelly mesenchymal stem cell paracrine signaling on keloid fibroblasts (pp. 299-307) https://doi.org/10.5966/sctm.2013-0120
  3. Bakhtyar et al. (2017) Acellular gelatinous material of human umbilical cord enhances wound healing: a candidate remedy for deficient wound healing https://doi.org/10.3389/fphys.2017.00200
  4. Beiki et al. (2017) Fabrication of a three dimensional spongy scaffold using human Wharton’s jelly derived extra cellular matrix for wound healing (pp. 627-638) https://doi.org/10.1016/j.msec.2017.04.074
  5. Benders et al. (2013) Extracellular matrix scaffolds for cartilage and bone regeneration (pp. 169-176) https://doi.org/10.1016/j.tibtech.2012.12.004
  6. Bhardwaj et al. (2011) Freeze-gelled silk fibroin protein scaffolds for potential applications in soft tissue engineering 49(3) (pp. 260-267) https://doi.org/10.1016/j.ijbiomac.2011.04.013
  7. Brown et al. (2011) Comparison of three methods for the derivation of a biologic scaffold composed of adipose tissue extracellular matrix (pp. 411-421) https://doi.org/10.1089/ten.tec.2010.0342
  8. Cha et al. (2013) Induction of re-differentiation of passaged rat chondrocytes using a naturally obtained extracellular matrix microenvironment (pp. 978-988) https://doi.org/10.1089/ten.tea.2012.0358
  9. Chao et al. (2010) Silk hydrogel for cartilage tissue engineering (pp. 84-90) https://doi.org/10.1002/jbm.b.31686
  10. Choi et al. (2012) Decellularized extracellular matrix derived from porcine adipose tissue as a xenogeneic biomaterial for tissue engineering (pp. 866-876) https://doi.org/10.1089/ten.tec.2012.0009
  11. Converse et al. (2017) Wharton’s jelly matrix decellularization for tissue engineering applications (pp. 1-9)
  12. Costa et al. (2007) Ross Operation with decelularized pulmonary allografts: medium-term results (pp. 454-462) https://doi.org/10.1590/S0102-76382007000400012
  13. Dan et al. (2017) Human-derived extracellular matrix from Wharton’s jelly: an untapped substrate to build up a standardized and homogeneous coating for vascular engineering (pp. 227-237) https://doi.org/10.1016/j.actbio.2016.10.018
  14. Ebrahimi-Barough et al. (2013) Programming of human endometrial-derived stromal cells (EnSCs) into pre-oligodendrocyte cells by overexpression of miR-219 (pp. 65-70) https://doi.org/10.1016/j.neulet.2013.01.022
  15. Ferguson and Dodson (2009) Bioengineering aspects of the umbilical cord (pp. S108-S113) https://doi.org/10.1016/j.ejogrb.2009.02.024
  16. Gilpin and Yang (2017) Decellularization strategies for regenerative medicine: from processing techniques to applications (pp. 1-13) https://doi.org/10.1155/2017/9831534
  17. Guziewicz et al. (2011) Lyophilized silk fibroin hydrogels for the sustained local delivery of therapeutic monoclonal antibodies (pp. 2642-2650) https://doi.org/10.1016/j.biomaterials.2010.12.023
  18. Hao et al. (2013) Culturing on Wharton’s jelly extract delays mesenchymal stem cell senescence through p53 and p16INK4a/pRb pathways https://doi.org/10.1371/journal.pone.0058314
  19. Hellström et al. (2014) Towards the development of a bioengineered uterus: comparison of different protocols for rat uterus decellularization (pp. 5034-5042) https://doi.org/10.1016/j.actbio.2014.08.018
  20. Herrero-Mendez et al. (2016) Generation of tunable glycosaminoglycan hydrogels to mimic extracellular matrices (pp. 1000-1011) https://doi.org/10.1002/term.1883
  21. Herrero-Mendez et al. (2017) HR007: a family of biomaterials based on glycosaminoglycans for tissue repair (pp. 989-1001) https://doi.org/10.1002/term.1998
  22. Hwang et al. (2017) Molecular assessment of collagen denaturation in decellularized tissues using a collagen hybridizing peptide (pp. 268-278) https://doi.org/10.1016/j.actbio.2017.01.079
  23. Jadalannagari et al. (2017) Decellularized Wharton’s Jelly from human umbilical cord as a novel 3D scaffolding material for tissue engineering applications https://doi.org/10.1371/journal.pone.0172098
  24. Kapoor and Kundu (2016) Silk protein-based hydrogels: promising advanced materials for biomedical applications (pp. 17-32) https://doi.org/10.1016/j.actbio.2015.11.034
  25. Khodadi et al. (2016) Bone marrow niche in immune thrombocytopenia: a focus on megakaryopoiesis (pp. 1765-1776) https://doi.org/10.1007/s00277-016-2703-1
  26. Kiyotake et al. (2016) Cartilage extracellular matrix as a biomaterial for cartilage regeneration (pp. 139-159) https://doi.org/10.1111/nyas.13278
  27. Kusuma et al. (2017) Effect of the microenvironment on mesenchymal stem cell paracrine signaling: opportunities to engineer the therapeutic effect (pp. 617-631) https://doi.org/10.1089/scd.2016.0349
  28. Law et al. (2016) Tissue-engineered trachea: a review (pp. 55-63) https://doi.org/10.1016/j.ijporl.2016.10.012
  29. Le Goff et al. (2015) Rheological study of reinforcement of agarose hydrogels by cellulose nanowhiskers (pp. 117-123) https://doi.org/10.1016/j.carbpol.2014.04.085
  30. Li et al. (2008) Silk fibroin-based scaffolds for tissue engineering 7(3) (pp. 237-247) https://doi.org/10.1007/s11706-013-0214-8
  31. Małkowski et al. (2008) TGF-β binding in human Wharton’s jelly (pp. 137-143) https://doi.org/10.1007/s11010-008-9704-x
  32. Meyer and Hargens (2012) Distribution and transport of fluid as related to tissue structure (pp. 25-46) Springer Science & Business Media
  33. Sekine et al. (2013) Chondrocyte differentiation of human endometrial gland-derived MSCs in layered cell sheets https://doi.org/10.1155/2013/359109
  34. Singh et al. (2016) Potential of agarose/silk fibroin blended hydrogel for in vitro cartilage tissue engineering (pp. 21236-21249) https://doi.org/10.1021/acsami.6b08285
  35. Sobolewski et al. (1997) Collagen and glycosaminoglycans of Wharton’s jelly (pp. 11-21) https://doi.org/10.1159/000244392
  36. Sobolewski et al. (2005) Wharton’s jelly as a reservoir of peptide growth factors (pp. 747-752) https://doi.org/10.1016/j.placenta.2004.10.008
  37. Sundaram et al. (2017) 3D decellularized native extracellular matrix scaffold for in vitro culture expansion of human Wharton’s jelly-derived mesenchymal stem cells (hWJ MSCs) https://doi.org/10.1007/7651_2017_71
  38. Swinehart and Badylak (2016) Extracellular matrix bioscaffolds in tissue remodeling and morphogenesis (pp. 351-360) https://doi.org/10.1002/dvdy.24379
  39. Taylor-Weiner et al. (2013) Defined extracellular matrix components are necessary for definitive endoderm induction (pp. 2084-2094) https://doi.org/10.1002/stem.1453
  40. Uebersax et al. (2008) Insulin-like growth factor I releasing silk fibroin scaffolds induce chondrogenic differentiation of human mesenchymal stem cells (pp. 12-21) https://doi.org/10.1016/j.jconrel.2007.11.006
  41. Verdi et al. (2014) Endometrial stem cells in regenerative medicine https://doi.org/10.1186/1754-1611-8-20
  42. Wang et al. (2008) Sonication-induced gelation of silk fibroin for cell encapsulation (pp. 1054-1064) https://doi.org/10.1016/j.biomaterials.2007.11.003
  43. Wolf and Friedl (2011) Extracellular matrix determinants of proteolytic and non-proteolytic cell migration (pp. 736-744) https://doi.org/10.1016/j.tcb.2011.09.006
  44. Wolff et al. (2007) Demonstration of multipotent stem cells in the adult human endometrium by in vitro chondrogenesis (pp. 524-533) https://doi.org/10.1177/1933719107306896
  45. Xiao et al. (2017) Fabrication and in vitro study of tissue-engineered cartilage scaffold derived from Wharton’s jelly extracellular matrix https://doi.org/10.1155/2017/5839071
  46. Yang et al. (2009) Fabrication and repair of cartilage defects with a novel acellular cartilage matrix scaffold (pp. 865-876) https://doi.org/10.1089/ten.tec.2009.0444
  47. Yucel et al. (2009) Vortex-induced injectable silk fibroin hydrogels (pp. 2044-2050) https://doi.org/10.1016/j.bpj.2009.07.028
  48. Zhao et al. (2018) hWJECM-derived oriented scaffolds with autologous chondrocytes for rabbit cartilage defect repairing (pp. 905-914) https://doi.org/10.1089/ten.tea.2017.0223
  49. Zubir and Pushpanathan (2016) Silk in biomedical engineering: a review (pp. 18-29)