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Stem Cells International
Volume 2014, Article ID 891518, 12 pages
http://dx.doi.org/10.1155/2014/891518
Research Article

Differentiation of Equine Mesenchymal Stromal Cells into Cells of Neural Lineage: Potential for Clinical Applications

1Department of Comparative and Experimental Medicine, University of Tennessee, Knoxville, TN 37996, USA
2Department of Large Animal Clinical Sciences, University of Tennessee, Knoxville, TN 37996, USA
3Department of Biomedical and Diagnostic Sciences, University of Tennessee, Knoxville, TN 37996, USA
4Advanced Microscopy and Imaging Center, University of Tennessee, Knoxville, TN 37996, USA

Received 25 July 2014; Revised 29 October 2014; Accepted 31 October 2014; Published 24 November 2014

Academic Editor: Peter J. Quesenberry

Copyright © 2014 Claudia Cruz Villagrán et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. W. Campbell, “Evaluation and management of peripheral nerve injury,” Clinical Neurophysiology, vol. 119, no. 9, pp. 1951–1965, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Forostyak, P. Jendelova, and E. Sykova, “The role of mesenchymal stromal cells in spinal cord injury, regenerative medicine and possible clinical applications,” Biochimie, vol. 95, no. 12, pp. 2257–2270, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Woodhoo, M. B. D. Alonso, A. Droggiti et al., “Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity,” Nature Neuroscience, vol. 12, no. 7, pp. 839–847, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. A. J. Cardozo, D. E. Gómez, and P. F. Argibay, “Neurogenic differentiation of human adipose-derived stem cells: relevance of different signaling molecules, transcription factors, and key marker genes,” Gene, vol. 511, no. 2, pp. 427–436, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. K. R. Jessen and R. Mirsky, “The origin and development of glial cells in peripheral nerves,” Nature Reviews Neuroscience, vol. 6, no. 9, pp. 671–682, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. D. P. Kuffler, “An assessment of current techniques for inducing axon regeneration and neurological recovery following peripheral nerve trauma,” Progress in Neurobiology, vol. 116, pp. 1–12, 2014. View at Google Scholar
  7. Y. Pan and S. Cai, “Current state of the development of mesenchymal stem cells into clinically applicable Schwann cell transplants,” Molecular and Cellular Biochemistry, vol. 368, no. 1-2, pp. 127–135, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. Z. Ren, Y. Wang, J. Peng, Q. Zhao, and S. Lu, “Role of stem cells in the regeneration and repair of peripheral nerves,” Reviews in the Neurosciences, vol. 23, no. 2, pp. 135–143, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Schaakxs, D. F. Kalbermatten, W. Raffoul, M. Wiberg, and P. J. Kingham, “Regenerative cell injection in denervated muscle reduces atrophy and enhances recovery following nerve repair,” Muscle and Nerve, vol. 47, no. 5, pp. 691–701, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. A. B. Spejo, J. L. Carvalho, A. M. Goes, and A. L. R. Oliveira, “Neuroprotective effects of mesenchymal stem cells on spinal motoneurons following ventral root axotomy: synapse stability and axonal regeneration,” Neuroscience, vol. 250, pp. 715–732, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Keilhoff, A. Goihl, K. Langnäse, H. Fansa, and G. Wolf, “Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells,” European Journal of Cell Biology, vol. 85, no. 1, pp. 11–24, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. G. Keilhoff, F. Stang, A. Goihl, G. Wolf, and H. Fansa, “Transdifferentiated mesenchymal stem cells as alternative therapy in supporting nerve regeneration and myelination,” Cellular and Molecular Neurobiology, vol. 26, no. 7-8, pp. 1235–1252, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Woodbury, E. J. Schwarz, D. J. Prockop, and I. B. Black, “Adult rat and human bone marrow stromal cells differentiate into neurons,” Journal of Neuroscience Research, vol. 61, no. 4, pp. 364–370, 2000. View at Google Scholar
  14. G. F. Barnabé, T. T. Schwindt, M. E. Calcagnotto et al., “Chemically-induced RAT mesenchymal stem cells adopt molecular properties of neuronal-like cells but do not have basic neuronal functional properties,” PLoS ONE, vol. 4, no. 4, Article ID e5222, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Bossio, R. Mastrangelo, R. Morini et al., “A simple method to generate adipose stem cell-derived neurons for screening purposes,” Journal of Molecular Neuroscience, vol. 51, no. 2, pp. 274–281, 2013. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Gong, Y. Bi, W. Jiang et al., “Retinoic acid receptor beta mediates all-trans retinoic acid facilitation of mesenchymal stem cells neuronal differentiation,” International Journal of Biochemistry and Cell Biology, vol. 45, no. 4, pp. 866–875, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. S. Wislet-Gendebien, P. Leprince, G. Moonen, and B. Rogister, “Regulation of neural markers nestin and GFAP expression by cultivated bone marrow stromal cells,” Journal of Cell Science, vol. 116, no. 16, pp. 3295–3302, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Muñoz-Elias, D. Woodbury, and I. B. Black, “Marrow stromal cells, mitosis, and neuronal differentiation: stem cell and precursor functions,” Stem Cells, vol. 21, no. 4, pp. 437–448, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. T. Himeno, H. Kamiya, K. Naruse et al., “Mesenchymal stem cell-like cells derived from mouse induced pluripotent stem cells ameliorate diabetic polyneuropathy in mice,” BioMed Research International, vol. 2013, Article ID 259187, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Nishida, M. Nakayama, H. Tanaka et al., “Evaluation of transplantation of autologous bone marrow stromal cells into the cerebrospinal fluid for treatment of chronic spinal cord injury in dogs,” American Journal of Veterinary Research, vol. 72, no. 8, pp. 1118–1123, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Voulgari-Kokota, R. Fairless, M. Karamita et al., “Mesenchymal stem cells protect CNS neurons against glutamate excitotoxicity by inhibiting glutamate receptor expression and function,” Experimental Neurology, vol. 236, no. 1, pp. 161–170, 2012. View at Publisher · View at Google Scholar · View at Scopus
  22. A.-T. Hameed, R. Ibrahim, A.-J. Karim, A. Zuki, T. Azmi, and R. Ramasamy, “Neurobiological observations of bone mesenchymal stem cells in vitro and in vivo of injured sciatic nerve in rabbit,” Journal of Animal and Veterinary Advances, vol. 10, no. 6, pp. 686–691, 2011. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Tremp, M. M. Schwabedissen, E. A. Kappos et al., “The regeneration potential after human and autologous stem cell transplantation in a rat sciatic nerve injury model can be monitored by MRI,” Cell Transplantation, 2013. View at Publisher · View at Google Scholar
  24. R. M. Stassart, R. Fledrich, V. Velanac et al., “A role for Schwann cell-derived neuregulin-1 in remyelination,” Nature Neuroscience, vol. 16, no. 1, pp. 48–54, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. J. L. Carter-Arnold, N. L. Neilsen, L. L. Amelse, A. Odoi, and M. S. Dhar, “In vitro analysis of equine, bone marrow-derived mesenchymal stem cells demonstrates differences within age- and gender-matched horses,” Equine Veterinary Journal, vol. 46, no. 5, pp. 589–595, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. Y. Kasashima, T. Ueno, A. Tomita, A. E. Goodship, and R. K. W. Smith, “Optimisation of bone marrow aspiration from the equine sternum for the safe recovery of mesenchymal stem cells,” Equine Veterinary Journal, vol. 43, no. 3, pp. 288–294, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. S. J. Arnhold, I. Goletz, H. Klein et al., “Isolation and characterization of bone marrow-derived equine mesenchymal stem cells,” American Journal of Veterinary Research, vol. 68, no. 10, pp. 1095–1105, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. G. C. Kopen, D. J. Prockop, and D. G. Phinney, “Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 19, pp. 10711–10716, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Bossolasco, L. Cova, C. Calzarossa et al., “Neuro-glial differentiation of human bone marrow stem cells in vitro,” Experimental Neurology, vol. 193, no. 2, pp. 312–325, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Hermann, S. Liebau, R. Gastl et al., “Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols,” Journal of Neuroscience Research, vol. 83, no. 8, pp. 1502–1514, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. N. Tremain, J. Korkko, D. Ibberson, G. C. Kopen, C. DiGirolamo, and D. G. Phinney, “MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAS of multiple cell lineages,” Stem Cells, vol. 19, no. 5, pp. 408–418, 2001. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Woodbury, K. Reynolds, and I. B. Black, “Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis,” Journal of Neuroscience Research, vol. 69, no. 6, pp. 908–917, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. J. R. Sanchez-Ramos, “Neural cells derived from adult bone marrow and umbilical cord blood,” Journal of Neuroscience Research, vol. 69, no. 6, pp. 880–893, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Hermann, R. Gastl, S. Liebau et al., “Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells,” Journal of Cell Science, vol. 117, no. 19, pp. 4411–4422, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, no. 5411, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. B. A. Reynolds, W. Tetzlaff, and S. Weiss, “A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes,” Journal of Neuroscience, vol. 12, no. 11, pp. 4565–4574, 1992. View at Google Scholar · View at Scopus
  37. J. Sanchez-Ramos, S. Song, F. Cardozo-Pelaez et al., “Adult bone marrow stromal cells differentiate into neural cells in vitro,” Experimental Neurology, vol. 164, no. 2, pp. 247–256, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. P.-F. Choong, P.-L. Mok, S.-K. Cheong, C.-F. Leong, and K.-Y. Then, “Generating neuron-like cells from BM-derived mesenchymal stromal cells in vitro,” Cytotherapy, vol. 9, no. 2, pp. 170–183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Tondreau, L. Lagneaux, M. Dejenefle et al., “Bone marrow-derived mesenchymal stem cells already express specific neural proteins before any differentiation,” Differentiation, vol. 72, no. 7, pp. 319–326, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. D. Foudah, M. Monfrini, E. Donzelli et al., “Expression of neural markers by undifferentiated mesenchymal-like stem cells from different sources,” Journal of Immunology Research, vol. 2014, Article ID 987678, 16 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. J.-L. Boulland, M. Mastrangelopoulou, A. C. Boquest et al., “Epigenetic regulation of nestin expression during neurogenic differentiation of adipose tissue stem cells,” Stem Cells and Development, vol. 22, no. 7, pp. 1042–1052, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. C. L. Hyder, K. O. Isoniemi, E. S. Torvaldson, and J. E. Eriksson, “Insights into intermediate filament regulation from development to ageing,” Journal of Cell Science, vol. 124, no. 9, pp. 1363–1372, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. X. Jin, J.-E. Jung, S. Beck, and H. Kim, “Cell surface Nestin is a biomarker for glioma stem cells,” Biochemical and Biophysical Research Communications, vol. 433, no. 4, pp. 496–501, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Michalczyk and M. Ziman, “Nestin structure and predicted function in cellular cytoskeletal organisation,” Histology and Histopathology, vol. 20, no. 2, pp. 665–671, 2005. View at Google Scholar · View at Scopus