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Differentiation of Human Endometrial Stem Cells into Schwann Cells in Fibrin Hydrogel as 3D Culture

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An Erratum to this article was published on 28 January 2016

Abstract

Human endometrial stem cells (hEnSCs) are a new source of adult multipotent stem cells with the ability of differentiation into many cell lineages. Many stem cell sources are desirable for differentiation into Schwann cells. Schwann-like cells derived from hEnSCs may be one of the ideal alternative cell sources for Schwann cell generation. In this study, for differentiation of hEnSCs into Schwann cells, hEnSCs were induced with RA/FSK/PDGF-AA/HRG as an induction medium for 14 days. The cells were cultured in a tissue culture plate (TCP) and fibrin gel matrix. The viability of cultured cells in the fibrin gel and TCP was analyzed with 3-[4,5-dimethyl-2-thia-zolyl]-2, 5-diphenyl-2H-tetrazolium bromide (MTT) assay for 7 days. The attachment of cells was analyzed with SEM and DAPI staining. The expression of S100 and P75 as Schwann cell markers was evaluated by immunocytochemistry and quantitative real-time PCR (RT-PCR). The evaluation of the MTT assay and gene expression showed that the survival rate and differentiation of hEnSCs into Schwann cells in the fibrin gel were better than those in the TCP group. These results suggest that human EnSCs can be differentiated into Schwann cells in the fibrin gel better than in the TCP, and the fibrin gel might provide a suitable three-dimensional (3D) scaffold for clinical applications for cell therapy of the nervous system.

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References

  1. Perale G, Rossi F, Sundstrom E, Bacchiega S, Masi M, Forloni G, Veglianese P (2011) Hydrogels in spinal cord injury repair strategies. ACS Chem Neurosci 2(7):336–345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Asmani MN, Ai J, Amoabediny G, Noroozi A, Azami M, Ebrahimi-Barough S, Navaei-Nigjeh M, Ai A, Jafarabadi M (2013) Three-dimensional culture of differentiated endometrial stromal cells to oligodendrocyte progenitor cells (OPCs) in fibrin hydrogel. Cell Biol Int 37(12):1340–1349

    Article  CAS  PubMed  Google Scholar 

  3. Kingham PJ, Kalbermatten DF, Mahay D, Armstrong SJ, Wiberg M, Terenghi G (2007) Adipose-derived stem cells differentiate into a Schwann cell phenotype and promote neurite outgrowth in vitro. Exp Neurol 207(2):267–274

    Article  CAS  PubMed  Google Scholar 

  4. Xiaosong GU, Fei D, Yumin Y, Jie L (2011) Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Prog Neurobiol 93(2):204–230

    Article  CAS  Google Scholar 

  5. Khaing ZZ, Schmidt CE (2012) Advances in natural biomaterials for nerve tissue repair. Neurosci Lett 519(2):103–114

    Article  CAS  PubMed  Google Scholar 

  6. Ishihara M, Mochizuki-Oda N, Iwatsuki K, KishimaH IY, Ohnishi O, Umegaki M, Yoshimine T (2011) A new three dimensional axonal outgrowth assay for central nervous system regeneration. J Neurosci Methods 198(2):181–186

    Article  PubMed  Google Scholar 

  7. Jessen KR, Mirsky R (1999) Developmental regulation in the Schwann cell lineage. Adv Exp Med Biol 468:3–12

    Article  CAS  PubMed  Google Scholar 

  8. Hall S (2005) The response to injury in the peripheral nervous system. J Bone Joint Surg Br 87:1309–1319

    Article  CAS  PubMed  Google Scholar 

  9. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411):143–147

    Article  CAS  PubMed  Google Scholar 

  10. Barry FP, Murphy JM (2004) Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36(4):568–584

    Article  CAS  PubMed  Google Scholar 

  11. Caddick J, Kingham PJ, Gardiner NJ, Wiberg M, Terenghi G (2006) Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54(8):840–849

    Article  PubMed  Google Scholar 

  12. Tohill M, Mantovani C, Wiberg M, Terenghi G (2004) Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci Lett 362(3):200–203

    Article  CAS  PubMed  Google Scholar 

  13. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H (2001) Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci 4(11):1771–1776

    Article  Google Scholar 

  14. Keilhoff G, Goihl A, Langnäse K, Fansa H, Wolf G (2006) Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells. Eur J Cell Biol 85(1):11–24

    Article  CAS  PubMed  Google Scholar 

  15. Ai J, Shahverdi AR, Ebrahimi-Barough S, Kouchesfehani HM, Heidari S, Roozafzoon R, Verdi J, Khoshzaban A (2012) Derivation of adipocytes from human endometrial stem cells (EnSCs). J Reprod Infertil 13(3):151–157

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Ebrahimi-Barough S, Kouchesfahani HM, Ai J, Massumi M (2013) Differentiation of human endometrial stromal cells into oligodendrocyte progenitor cells (OPCs). J Mol Neurosci 51(2):265–273

  17. Bockeria L, Bogin V, Bockeria O, Le T, Alekyan B, Woods EJ, Brown A, Ichim TE, Amit PN (2013) Endometrial regenerative cells for treatment of heart failure: a new stem cell enters the clinic. J Trans Med 11:56

    Article  Google Scholar 

  18. Ebrahimi-Barough S, Massumi M, Kouchesfahani HM, Ai J (2013) Derivation of pre-oligodendrocytes from human endometrial stromal cells by using overexpression of microRNA 338. J Mol Neurosci 51(2):337–343

    Article  CAS  PubMed  Google Scholar 

  19. Ishihara M, Mochizuki-Oda N, Iwatsuki K, Kishima H, Iwamoto Y, Ohnishi O, Umegaki M, Yoshimine T (2011) A new three-dimensional axonal outgrowth assay for central nervous system regeneration. J Neurosci Methods 198(2):181–186

    Article  PubMed  Google Scholar 

  20. Niknamasl A, Ostad SN, Soleimani M, Azami M, Salmani MK, Lotfibakhshaiesh N, Ebrahimi-Barough S, Karimi R, Roozafzoon R, Ai J (2014) A new approach for pancreatic tissue engineering: human endometrial stem cells encapsulated in fibrin gel can differentiate to pancreatic islet beta-cell. Cell Biol Int 38(10):1174–1182

    Article  CAS  PubMed  Google Scholar 

  21. Xiaosong GU, Fei D, Yumin Y, Jie L (2011) Construction of tissue engineered nerve grafts and their application in peripheral nerve regeneration. Prog Neurobiol 93(2):204–230

    Article  CAS  Google Scholar 

  22. Ziv-Polat O, Skaat H, Shahar A, Margel S (2012) Novel magnetic fibrin hydrogel scaffolds containing thrombin and growth factors conjugated iron oxide nanoparticles for tissue engineering. Int J Nanomedicine 7:1259–1274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Laurens N, Koolwijk P, de-Maat MPM (2006) Fibrin structure and wound healing. J Thromb Haemost 4:932–939

    Article  CAS  PubMed  Google Scholar 

  24. Mosesson MW, Siebenlist KR, Meh DA (2001) The structure and biological features of fibrinogen and fibrin. Ann NY Acad Sci 936:11–30

    Article  CAS  PubMed  Google Scholar 

  25. Navaei-Nigjeh M, Amoabedini G, Noroozi A, Azami M, Asmani MN, Ebrahimi-Barough S, Saberi H, Ai A, Ai J (2014) Enhancing neuronal growth from human endometrial stem cells derived neuron-like cells in three-dimensional fibrin gel for nerve tissue engineering. J Biomed Mater Res A 102(8):2533–2543

    Article  CAS  PubMed  Google Scholar 

  26. Ai J, Kiasat-Dolatabadi A, Ebrahimi-Barough S, Ai A, Lotfibakhshaiesh N, Norouzi-Javidan A, Saberi H, Arjmand B, Aghayan HA (2014) Polymeric scaffolds in neural tissue engineering: a review. Archives of Neuroscience 1(1):15–20

    Article  Google Scholar 

  27. Yasuda H, Kuroda S, Shichinohe H, Kamei S, Kawamura R, Iwasaki Y (2010) Effect of biodegradable fibrin scaffold on survival, migration, and differentiation of transplanted bone marrow stromal cells after cortical injury in rats. J Neurosurg 112:336–344

    Article  CAS  PubMed  Google Scholar 

  28. Ebrahimi-Barough S, Hoveizi E, Norouzi Javidan A, Ai J (2015) Investigating the neuroglial differentiation effect of neuroblastoma conditioned medium in human endometrial stem cells cultured on 3D nanofibrous scaffold. Journal of Biomedical Materials Research Part A 103(8):2621–2627

    Article  CAS  PubMed  Google Scholar 

  29. Hoveizi E, Tavakol S, Ebrahimi-Barough S (2015) Neuroprotective effect of transplanted neural precursors embedded on PLA/CS scaffold in an animal model of multiple sclerosis. Mol neurobiol 51(3):1334–1342

    Article  CAS  PubMed  Google Scholar 

  30. Karin S, Foo S, Cheryl WP, Heilshorn SC (2010) Biomaterial design strategies for the treatment of spinal cord injuries. Neurotra 27(1):1–19

    Article  Google Scholar 

  31. Ebrahimi-Barough S, Norouzi Javidan A, Saberi H, Joghataei MT, Rahbarghazi R, Mirzaei E, Faghihi F, Shirian S, Ai A, Ai J (2015) Evaluation of motor neuron-like cell differentiation of hEnSCs on biodegradable PLGA nanofiber scaffolds. Mol Neurobiol 52(3):1704–1713

  32. Schwab KE, Gargett CE (2007) Co-expression of two perivascular cell markers isolates mesenchymal stem-like cells from human endometrium. Hum Reprod 22:2903–2911

    Article  CAS  PubMed  Google Scholar 

  33. Schuldiner M, Yanuka O, Itskovitz-Elder J, Melton DA, Benvenisty N (2000) Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 97:11307–11312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Deng W, Obrocka M, Fischer I, Prockop DJ (2001) In vitro differentiation of human marrow stromal cells into early progenitors of neural cells by conditions that increase intracellular cyclic AMP. Biochem Biophys Res Commun 282:148–152

    Article  CAS  PubMed  Google Scholar 

  35. Harirchian MH, Tekieh AH, Modabbernia A, Aghamollaii V, Tafakhori A, Ghaffarpour M, Sahraian MA, Naji M, Yazdankhah M (2012) Serum and CSF PDGF-AA and FGF-2 in relapsing-remitting multiple sclerosis: a case–control study. Eur J Neurol 19(2):241–247

    Article  CAS  PubMed  Google Scholar 

  36. Fraichard A, Chassande O, Bilbaut G, Dehay C, Savatier P, Samarut J (1995) In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J Cell Sci 108:3181–3188

    CAS  PubMed  Google Scholar 

  37. Yazdankhah M, Farioli-Vecchioli S, Tonchev AB, Stoykova A, Cecconi F (2014) The autophagy regulators Ambra1 and Beclin 1 are required for adult neurogenesis in the brain subventricular zone. Cell Death Dis 4(5):e1403. doi:10.1038/cddis.2014.358

    Article  CAS  Google Scholar 

  38. Liu J, Zhang Z, Gong A, Cao X, Qian L, Duan L, Sun X, Bu X (2010) Neuronal progenitor cells seeded in fibrin gel differentiate into ChAT-positive neuron. In Vitro Cell Dev Biol Animal 46:738–745

    Article  Google Scholar 

  39. Ju YE, Janmey PA, Mccormick ME, Sawyer ES, Flanagan LA (2007) Enhanced neurite growth from mammalian neurons in three-dimensional salmon fibrin gels. Biomaterials 28:2097–2108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Tavakol S, Aligholi H, Gorji A, Eshaghabadi A, Hoveizi E, Tavakol B, Rezayat SM, Ai J (2014) Thermogel nanofiber induces human endometrial-derived stromal cells to neural differentiation: in vitro and in vivo studies in rat. J Biomed Mater Res A 102(12):4590–4597

    PubMed  Google Scholar 

Download references

Acknowledgments

This research has been supported by Iran National Science Foundation (INSF) grant number 91042417.

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Authors and Affiliations

  1. Brain and Spinal Cord Injury Research Center (BASIR), Tehran University of Medical Sciences, Keshavarz Boulevard, Gharib Street, 6114185, Tehran, Iran

    Neda Bayat & Jafar Ai

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

    Somayeh Ebrahimi-Barough, Mohammad Mehdi Mokhtari Ardakan, Niloofar Babaloo & Jafar Ai

  3. School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

    Arman Ai

  4. Department of Genetics, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Ahmadreza Kamyab

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  1. Neda Bayat
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  2. Somayeh Ebrahimi-Barough
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Correspondence to Somayeh Ebrahimi-Barough or Jafar Ai.

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An erratum to this article is available at http://dx.doi.org/10.1007/s12035-016-9730-8.

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Bayat, N., Ebrahimi-Barough, S., Ardakan, M.M.M. et al. Differentiation of Human Endometrial Stem Cells into Schwann Cells in Fibrin Hydrogel as 3D Culture. Mol Neurobiol 53, 7170–7176 (2016). https://doi.org/10.1007/s12035-015-9574-7

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  • DOI: https://doi.org/10.1007/s12035-015-9574-7

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