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Molecular Neurobiology

, Volume 53, Issue 3, pp 1862–1872 | Cite as

Differentiation Potential of Human Chorion-Derived Mesenchymal Stem Cells into Motor Neuron-Like Cells in Two- and Three-Dimensional Culture Systems

  • Faezeh Faghihi
  • Esmaeil Mirzaei
  • Jafar Ai
  • Abolfazl Lotfi
  • Forough Azam Sayahpour
  • Somayeh Ebrahimi Barough
  • Mohammad Taghi JoghataeiEmail author
Article

Abstract

Many people worldwide suffer from motor neuron-related disorders such as amyotrophic lateral sclerosis and spinal cord injuries. Recently, several attempts have been made to recruit stem cells to modulate disease progression in ALS and also regenerate spinal cord injuries. Chorion-derived mesenchymal stem cells (C-MSCs), used to be discarded as postpartum medically waste product, currently represent a class of cells with self renewal property and immunomodulatory capacity. These cells are able to differentiate into mesodermal and nonmesodermal lineages such as neural cells. On the other hand, gelatin, as a simply denatured collagen, is a suitable substrate for cell adhesion and differentiation. It has been shown that electrospinning of scaffolds into fibrous structure better resembles the physiological microenvironment in comparison with two-dimensional (2D) culture system. Since there is no report on potential of human chorion-derived MSCs to differentiate into motor neuron cells in two- and three-dimensional (3D) culture systems, we set out to determine the effect of retinoic acid (RA) and sonic hedgehog (Shh) on differentiation of human C-MSCs into motor neuron-like cells cultured on tissue culture plates (2D) and electrospun nanofibrous gelatin scaffold (3D).

Keywords

Motor neuron Chorion Mesenchymal stem cells Electrospinning Gelatin 

Notes

Acknowledgments

This study was financially supported by grant no. 92004328 from Iran National Science Foundation (INSF) and Cellular-Molecular Research Center of Iran University of Medical Sciences.

Conflict of Interest

The authors declare that they have no conflict of interest.

Compliance with Ethical Standards

After full-term delivery, human chorion-derived mesenchymal stem cells were collected from placenta tissues of new born babies. The protocol to obtain and use of the cells in research were approved by the ethical committee of Iran University of Medical Sciences, after obtaining maternal informed consent.

References

  1. 1.
    Friedenstein AJ (1973) Determined and inducible osteogenic precursure cells. Hard Tissue Growth, Repair and Remineralization 169-185Google Scholar
  2. 2.
    Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM (2002) Human bone marrow stromal cells suppress Tlymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838–3843CrossRefPubMedGoogle Scholar
  3. 3.
    Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, Deans RJ, McIntosh KR (2005) T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci 12:47–57CrossRefPubMedGoogle Scholar
  4. 4.
    Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas JD (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147CrossRefPubMedGoogle Scholar
  5. 5.
    Sanchez-Ramos J, Song S, Cardozo-Pelaez F, Hazzi C, Stedeford T, Willing A, Freeman TB, Saporta S, Janssen W, Patel N (2000) Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp Neurol 164:247–256CrossRefPubMedGoogle Scholar
  6. 6.
    Zhao LR, Duan WM, Reyes M, Keene CD, Verfaillie CM, Low WC (2002) Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol 174:11–20CrossRefPubMedGoogle Scholar
  7. 7.
    Heary RF, Schlenk RP, Sacchieri TA, Barone D, Brotea C (2002) Persistent iliac crest donor site pain: independent outcome assessment. Neurosurgery 50:510–516PubMedGoogle Scholar
  8. 8.
    Nakajima T, Iizuka H, Tsutsumi S, Kayakabe M, Takagishi K (2007) Evaluation of posterolateral spinal fusion using mesenchymal stem cells: differences with or without osteogenic differentiation. Spine 32:2432–2436CrossRefPubMedGoogle Scholar
  9. 9.
    Barlow S, Brooke G, Chatterjee K, Price G, Pelekanos R, Rossetti T et al (2008) Comparison of human placenta-and bone marrow-derived multipotent mesenchymal stem cells. Stem Cells Dev 17:1095–1107CrossRefPubMedGoogle Scholar
  10. 10.
    Anker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE et al (2004) Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 22:1338–1345CrossRefGoogle Scholar
  11. 11.
    Koo BK, Park IY, Kim J et al (2012) Isolation and characterization of chorionic mesenchymal stromal cells from human full term placenta. J Korean Med Sci 27:857–863CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Ilancheran S, Moodley Y, Manuelpillai U (2009) Human fetal membranes: a source of stem cells for tissue regeneration and repair? Placenta 30:2–10CrossRefPubMedGoogle Scholar
  13. 13.
    Resca E, Zavatti M, Bertoni L, Maraldi T, De Biasi S, Pisciotta A, Nicoli A, La Sala GB, Guillot PV, David AL, Sebire NJ, De Coppi P, De Pol A (2013) Enrichment in c-Kit + enhances mesodermal and neural differentiation of human chorionic placental cells. Placenta 34:526–535CrossRefPubMedGoogle Scholar
  14. 14.
    Jiang G, Di Bernardo J, DeLong CJ, Monteiro da Rocha A, O’Shea KS, Kunisaki SM (2014) Induced pluripotent stem cells from human placental chorion for perinatal tissue engineering applications. Tissue Eng C Methods 20:731–740CrossRefGoogle Scholar
  15. 15.
    Novitch B, Wichterle H, Jessell T, Sockanathan S (2003) A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 40:81–95CrossRefPubMedGoogle Scholar
  16. 16.
    Briscoe J, Chen Y, Jessell TM, Struhl G (2001) A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol Cell 7:1279–1291CrossRefPubMedGoogle Scholar
  17. 17.
    Karumbayaram S, Novitch BG, Patterson M, Umbach JA, Richter L, Lindgren A (2009) Directed differentiation of human-induced pluripotent stem cells generates active motor neurons. Stem Cells 27:806–811CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385–397CrossRefPubMedGoogle Scholar
  19. 19.
    Hajiali H, Shahgasempour S, Naimi-Jamal MR, Peirovi H (2011) Electrospun PGA/gelatin nanofibrous scaffolds and their potential application in vascular tissue Engineering. Int J Nanomedicine 6:2133–2141CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ozeki M, Tabata Y (2005) In vivo degradability of hydrogels prepared from different gelatins by various crosslinking method. J Biomater Sci Polym 16:549–561CrossRefGoogle Scholar
  21. 21.
    Griffith LG, Swartz MA (2006) Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 7:211–224CrossRefPubMedGoogle Scholar
  22. 22.
    Abbott A (2003) Cell culture: biology’s new dimension. Nature 424:870–872CrossRefPubMedGoogle Scholar
  23. 23.
    Skotak M, Noriega S, Larsen G, Subramanian A (2010) Electrospun cross-linked gelatin fibers with controlled diameter: the effect of matrix stiffness on proliferative and biosynthetic activity of chondrocytes cultured in vitro. J Biomed Mater Res A 95:828–836CrossRefPubMedGoogle Scholar
  24. 24.
    Sisson K, Zhang C, Farach- Carson MC, Bruce Chase D, Rabolt JF (2009) Evaluation of cross-linking methods for electrospun gelatin on cell growth and viability. Biomacromolecules 10(7):1675–1680CrossRefPubMedGoogle Scholar
  25. 25.
    Baiguera S, Del Guadio C, Lucatelli E, Kuevda E, Boieri M, Mazzanti B, Bianco A, Macchiarini P (2014) Electrospun gelatin scaffolds incorporating rat decellularized brain extracellular matrix for neural tissue engineering. Biomaterials 35:1205–1214CrossRefPubMedGoogle Scholar
  26. 26.
    Ghasemi-mobarakeh L, Prabhakaran MP, Morshed M, Nasr-esfahani MH, Ramakrishnan S (2008) Electrospun poly(epsilon-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29P:4532–4539CrossRefGoogle Scholar
  27. 27.
    Nizzardo M, Simone C, Falcone M, Locatelli F, Riboldi G, Comi GP, Corti S (2010) Human motor neuron generation from embryonic stem cells and induced pluripotent stem cells. Cell Mol Life Sci 67:3837–3847CrossRefPubMedGoogle Scholar
  28. 28.
    Hedlund E, Hefferan MP, Marsala M, Isacson O (2007) Cell therapy and stem cells in animal models of motor neuron disorders. Eur J Neurosci 26:1721–1737CrossRefPubMedGoogle Scholar
  29. 29.
    Zhang X, Mitsuru A, Igura K et al (2006) Mesenchymal progenitor cells derived from chorionic villi of human placenta for cartilage tissue engineering. Biochem Biophys Res Commun 340:944–952CrossRefPubMedGoogle Scholar
  30. 30.
    Maden M (2002) Retinoid signalling in the development of the central nervous system. Nat Rev Neurosci 3:843–853CrossRefPubMedGoogle Scholar
  31. 31.
    Ericson J, Rashbass P, Schedl A, Brenner-Morton S, Kawakami A (1997) Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90:169–180CrossRefPubMedGoogle Scholar
  32. 32.
    Li XJ, Hu BY, Jones SA, Zhang YS, Lavaute T, Du ZW, Zhang SC (2008) Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 26(4):886–893CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Lee SK, Paff SL (2003) Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38:731–745CrossRefPubMedGoogle Scholar
  34. 34.
    Brejot T, Blanchard S, Hocquemiller M, Haase G (2006) Forced expression of the motor neuron determinant HB9 in neural stem cells affects neurogenesis. Exp Neurol 198:167–182CrossRefPubMedGoogle Scholar
  35. 35.
    Thaler JP, Koo SJ, Kania A, Lettieri K, Andrews S (2004) A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41:337–350CrossRefPubMedGoogle Scholar
  36. 36.
    Park HW, Cho JS, Park CK, Jung SJ, Park CH (2012) Directed induction of functional motor neuron-like cells from genetically engineered human mesenchymal stem cells. PLoS ONE 7:35244CrossRefGoogle Scholar
  37. 37.
    Ebrahimi-Barough S, Norouzi Javidan A, Saberi H, Joghataei MT, Rahbarghazi R, Mirzaei E, Faghihi F, Shirian S et al. (2014) Evaluation of motor neuron-like cell differentiation of hEnSCs on biodegradable PLGA nanofiber scaffolds. Molecular Neurobiology [Epub ahead of print]Google Scholar
  38. 38.
    Mota A, Sahebghadam Lotfi A, Barzin J, Hatam M, Adibi M, Khalaj Z, Massumi M (2014) Human bone marrow mesenchymal stem cell behaviors on PCL/gelatin nanofibrous scaffolds modified with a collagen IV-derived RGD-containing peptide. Cell J 16:1–10PubMedPubMedCentralGoogle Scholar
  39. 39.
    Ratanavaraporn J, Damrongsakkul S, Sanchavanakitn N, Banaprasert T, Kanokpanont S (2006) Comparison of gelatin and collagen scaffolds for fibroblast cell culture. J Met Mater Miner 16:31–36Google Scholar
  40. 40.
    Shahbazi E, Kiani S, Gourabi H, Baharvand H (2011) Electrospun nanofibrillar surfaces promote neuronal differentiation and function from human embryonic stem cells. Tissue Eng A 17:3021–3031CrossRefGoogle Scholar
  41. 41.
    Faghihi F, Mirzaei E, Sarveazad A, Ai J, Barough SE, Lotfi A, Joghataei MT (2014) Differentiation potential of human bone marrow mesenchymal stem cells into motorneuron-like cells on electrospun gelatin membrane. J Mol Neurosci. doi: 10.1007/s12031-014-0437-x PubMedGoogle Scholar
  42. 42.
    Liqing Y, Jia G, Jiqing C, Ran G, Fei C, Jie K, Yanyun W, Cheng (2011) Directed differentiation of motorneuron cell- like cells from human adipose-derived stem cells in vitro. Neuroreport 22(8):370–373CrossRefPubMedGoogle Scholar
  43. 43.
    Martín-López E, Nieto-Díaz M, Nieto-Sampedro M (2012) Differential adhesiveness and neurite-promoting activity for neural cells of chitosan, gelatin, and poly-L-lysine films. J Biomater Appl 26:791–809CrossRefPubMedGoogle Scholar
  44. 44.
    Liou HM, Rau LR, Huang C (2013) Electrospun hyaluronan-gelatin nanofibrous matrix for nerve tissue engineering. J Nanomater 613-628Google Scholar
  45. 45.
    Huimin Y, Lei Z, Yunfang W, Feng L, Lidong G, Shaoqing L, Fang Y, Xue N, Cixian B, Feng L, Yongnian Y, Xuetao P (2006) Proliferation and differentiation into endothelial cells of human bone marrow mesenchymal stem cells (MSCs) on poly DL-lactic-co-glycolic acid (PLGA) films. Sci Bull 51(1):1328–1333Google Scholar
  46. 46.
    Sockanathan S, Jessell TM (1998) Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94:503–514CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Faezeh Faghihi
    • 1
  • Esmaeil Mirzaei
    • 2
  • Jafar Ai
    • 3
    • 4
  • Abolfazl Lotfi
    • 5
  • Forough Azam Sayahpour
    • 6
  • Somayeh Ebrahimi Barough
    • 3
  • Mohammad Taghi Joghataei
    • 1
    • 7
    • 8
    Email author
  1. 1.Cellular and Molecular Research CenterIran University of Medical SciencesTehranIran
  2. 2.Department of Medical Nanotechnology, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
  3. 3.Department of Tissue Engineering, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
  4. 4.Brain and Spinal Injury Research CenterImam Khomeini Hospital, Tehran University of Medical SciencesTehranIran
  5. 5.Department of BiotechnologyNational Institute of Genetic Engineering and BiotechnologyTehranIran
  6. 6.Department of Stem Cells and Developmental Biology at Cell Science Research CenterRoyan Institute for Stem Cell Biology and Technology, ACECRTehranIran
  7. 7.Department of Neuroscience, School of Advanced Technologies in MedicineIran University of Medical SciencesTehranIran
  8. 8.Department of Anatomy, School of MedicineIran University of Medical SciencesTehranIran

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