Advertisement

Journal of Molecular Neuroscience

, Volume 55, Issue 4, pp 845–853 | Cite as

Differentiation Potential of Human Bone Marrow Mesenchymal Stem Cells into Motorneuron-like Cells on Electrospun Gelatin Membrane

  • Faezeh Faghihi
  • Esmaeil Mirzaei
  • Arash Sarveazad
  • Jafar Ai
  • Somayeh Ebrahimi Barough
  • Abolfazl Lotfi
  • Mohammad Taghi Joghataei
Article

Abstract

Human bone marrow-derived mesenchymal stem cells are potent types of cells with self renewal ability and immunomodulatory properties. They not only have the capacity to differentiate into mesodermal lineages, but they are also capable to transdifferentiate into neural cells in vitro and in vivo. From a biological point of view, the specification of cell fate in the central nervous system is largely dictated by retinoic acid and sonic hedgehog. In addition with inductive molecules, electrospun three dimensional (3D) scaffolds with similar properties to natural extracellular matrix represent a physiological environment that could better resemble the in vivo microenvironment in comparison with two dimensional culture systems. In this regard, the aim of this study was to examine whether induction of human BM-MSCs with retinoic acid (RA) and sonic hedgehog (Shh) in combination with electrospun gelatin scaffold could lead to better differentiation of human bone marrow-derived mesenchymal stem cells (hBM-MSCs) into motorneuron-like cells in vitro.

Keywords

Human bone marrow mesenchymal stem cells Motorneuron Electrospun gelatin membrane 

Notes

Acknowledgments

This study was financially supported by Iran National Science Foundation (INSF).

Conflicts of Interest

The authors declare that they have no conflicts of interest.

References

  1. Abbott A (2003) Cell culture: biology’s new dimension. Nature 424:870–872CrossRefPubMedGoogle Scholar
  2. 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(4):1205–1214CrossRefPubMedGoogle Scholar
  3. Bassi EJ, Aita CAM, Câmara NOS (2011) Immune regulatory properties of multipotent mesenchymal stromal cells: where do we stand? World J Stem Cells 3:1–8CrossRefPubMedCentralPubMedGoogle Scholar
  4. 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
  5. 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
  6. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40:65–79CrossRefPubMedGoogle Scholar
  7. 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
  8. Faghihi F, Baghaban Eslaminejad M, Nekookar A, Najar M, Salekdeh GH (2013) The effect of purmorphamine and sirolimus on osteogenic differentiation of human bone marrow-derived mesenchymal stem cells. Biomed Pharmacother 67:31–38CrossRefPubMedGoogle Scholar
  9. Friedenstein AJ, Piatetzky-Shapiro II, Petrakova KV (1966) Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 16:381–390PubMedGoogle Scholar
  10. Ghasemi-obarakeh L, Prabhakaran MP, Morshed M, Nasr-esfahani MH, Ramakrishnan S (2008) Electrospun poly(epsilon-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29(34):4532–4539CrossRefGoogle Scholar
  11. Griffith LG, Swartz MA (2006) Capturing complex 3D tissue physiology in vitro. Nat Rev Mol Cell Biol 7(3):211–24CrossRefPubMedGoogle Scholar
  12. 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 6:2133–2141CrossRefPubMedCentralPubMedGoogle Scholar
  13. Hermann A, Gastl R, Liebau S, Oana Popa M, Fiedler J, Boehm BO, Maisel M, Lerche H, Schwarz J, Brenner R, Storch A (2004) Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117:4411–4422CrossRefPubMedGoogle Scholar
  14. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR, Pittenger MF (2000) Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. J Biol Chem 275:9645–52CrossRefPubMedGoogle Scholar
  15. Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20–29CrossRefPubMedGoogle Scholar
  16. 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 27:806–811CrossRefPubMedCentralPubMedGoogle Scholar
  17. 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
  18. Liou HM, Rau LR, Huang CC, Lu (2013) Electrospun Hyaluronan- gelatin nanofibrous matrix for nerve tissue engineering. J Nanomaters, 613–628Google Scholar
  19. Liqing Y, Jia G, Jiqing C, Ran G, Fei C, Jie K, Yanyun W, Cheng Z (2011) Directed differentiation of motor neuron cell-like cells from human adipose-derived stem cells in vitro. NeuroReport 22:370–373CrossRefPubMedGoogle Scholar
  20. Maden M (2002) Retinoid signalling in the development of the central nervous system. Nat Rev Neurosci 3:843–853CrossRefPubMedGoogle Scholar
  21. 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(7):791–809CrossRefPubMedGoogle Scholar
  22. 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):1–10PubMedCentralPubMedGoogle Scholar
  23. 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
  24. Ozeki M, Tabata Y (2005) In vivo degradability of hydrogels prepared from different gelatins by various crosslinking method. J Biomater Sci Polym Ed 16(5):549–561CrossRefPubMedGoogle Scholar
  25. 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(4):e35244CrossRefPubMedCentralPubMedGoogle Scholar
  26. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas JD (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147CrossRefPubMedGoogle Scholar
  27. Ratanavaraporn J, Damrongsakkul S, Sanchavanakit N, Banaprasert T, Kanokpanont S (2006) Comparison of gelatin and collagen scaffolds for fibroblast cell culture. J Metals Mater Miner 16:31–36Google Scholar
  28. 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
  29. Schacter DL, Gilbert DT, Wegner DM (2011) Psychology, 2nd ed., New YorkGoogle Scholar
  30. Schwartz PH (2006) The potential of Stm cell therapies for neurological diseases. Expert Rev Neurother 6(2):153–161CrossRefPubMedGoogle Scholar
  31. 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(23–24):3021–3031CrossRefGoogle Scholar
  32. Sisson K, Zhang C, Farach-Carson MC, Chase B, Rabolt JF (2009) Evaluation of cross-linking methods for electrospun gelatin on cell growth and viability. Biomacromolecules 10(7):1675–1680CrossRefPubMedGoogle Scholar
  33. 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 95a(3):828–836CrossRefGoogle Scholar
  34. Sockanathan S, Jessell TM (1998) Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94:503–514CrossRefPubMedGoogle Scholar
  35. Solchaga LA, Penick KJ, Welter JF (2011) Chondrogenic differentiation of bone marrow-derived mesenchymal stem cells: tips and tricks. Methods Mol Biol 698:253–78CrossRefPubMedCentralPubMedGoogle Scholar
  36. 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
  37. Wichterle H, Lieberam I, Porter JA, Jessell TM (2002) Directed differentiation of embryonic stem cells into motor neurons. Cell 110:385–397CrossRefPubMedGoogle Scholar
  38. Woodbury D, Reynolds K, Black B (2002) Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J Neurosci Res 69(6):908–917CrossRefPubMedGoogle Scholar
  39. Zhang YZ, Venugopal J, Huang ZM, Lim CT, Ramakrishna S (2006) Crosslinking of the electrospun gelatin nanofibers. Polymer 47:2911–2917CrossRefGoogle Scholar
  40. 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

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Faezeh Faghihi
    • 1
  • Esmaeil Mirzaei
    • 2
  • Arash Sarveazad
    • 3
  • Jafar Ai
    • 4
    • 5
  • Somayeh Ebrahimi Barough
    • 4
  • Abolfazl Lotfi
    • 6
  • Mohammad Taghi Joghataei
    • 1
    • 3
    • 7
  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 Anatomy, School of MedicineIran University of Medical SciencesTehranIran
  4. 4.Department of Tissue Engineering, School of Advanced Technologies in MedicineTehran University of Medical SciencesTehranIran
  5. 5.Brain and Spinal Injury Research Center, Imam Khomeini HospitalTehran University of Medical SciencesTehranIran
  6. 6.Department of BiotechnologyNational Institute of Genetic Engineering and BiotechnologyTehranIran
  7. 7.Department of Neuroscience, School of Advanced Technologies in MedicineIran University of Medical SciencesTehranIran

Personalised recommendations