Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2015 (2015), Article ID 516215, 13 pages
http://dx.doi.org/10.1155/2015/516215
Research Article

The Cotransplantation of Olfactory Ensheathing Cells with Bone Marrow Mesenchymal Stem Cells Exerts Antiapoptotic Effects in Adult Rats after Spinal Cord Injury

1Department of Orthopedics, Linyi People’s Hospital Affiliated to Shandong University, Linyi, Shandong 276000, China
2Respiratory Department, Qilu Children’s Hospital of Shandong University, Jinan, Shandong 250022, China
3Department of Toxicology, Shandong Academy of Occupational Health and Occupational Medicine, Shandong Academy of Medical Sciences, Jinan, Shandong 250062, China
4National Research Centre for Environmental Toxicology (Entox), The University of Queensland, Brisbane, QLD 4108, Australia

Received 18 April 2015; Revised 24 June 2015; Accepted 29 June 2015

Academic Editor: Jianglin Fan

Copyright © 2015 Shifeng Wu 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. V. R. Dasari, D. G. Spomar, C. Cady, M. Gujrati, J. S. Rao, and D. H. Dinh, “Mesenchymal stem cells from rat bone marrow downregulate caspase-3-mediated apoptotic pathway after spinal cord injury in rats,” Neurochemical Research, vol. 32, no. 12, pp. 2080–2093, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Torres-Espín, E. Redondo-Castro, J. Hernández, and X. Navarro, “Bone marrow mesenchymal stromal cells and olfactory ensheathing cells transplantation after spinal cord injury—a morphological and functional comparison in rats,” European Journal of Neuroscience, vol. 39, no. 10, pp. 1704–1717, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. A. J. Mothe and C. H. Tator, “Advances in stem cell therapy for spinal cord injury,” Journal of Clinical Investigation, vol. 122, no. 11, pp. 3824–3834, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. J. D. Kocsis, K. L. Lankford, M. Sasaki, and C. Radtke, “Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury,” Neuroscience Letters, vol. 456, no. 3, pp. 137–142, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. C. L. Beites, S. Kawauchi, C. E. Crocker, and A. L. Calof, “Identification and molecular regulation of neural stem cells in the olfactory epithelium,” Experimental Cell Research, vol. 306, no. 2, pp. 309–316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. C. T. Marshall, C. Lu, W. Winstead et al., “The therapeutic potential of human olfactory-derived stem cells,” Histology and Histopathology, vol. 21, no. 4–6, pp. 633–643, 2006. View at Google Scholar · View at Scopus
  7. R. López-Vales, J. Forés, E. Verdú, and X. Navarro, “Acute and delayed transplantation of olfactory ensheathing cells promote partial recovery after complete transection of the spinal cord,” Neurobiology of Disease, vol. 21, no. 1, pp. 57–68, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. M. I. Chuah, D. M. Hale, and A. K. West, “Interaction of olfactory ensheathing cells with other cell types in vitro and after transplantation: glial scars and inflammation,” Experimental Neurology, vol. 229, no. 1, pp. 46–53, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Torres-Espín, J. Hernández, and X. Navarro, “Gene expression changes in the injured spinal cord following transplantation of mesenchymal stem cells or olfactory ensheathing cells,” PLoS ONE, vol. 8, no. 10, Article ID e76141, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. J. C. Stamegna, M. S. Felix, J. Roux-Peyronnet et al., “Nasal OEC transplantation promotes respiratory recovery in a subchronic rat model of cervical spinal cord contusion,” Experimental Neurology, vol. 229, no. 1, pp. 120–131, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Boido, D. Garbossa, M. Fontanella, A. Ducati, and A. Vercelli, “Mesenchymal stem cell transplantation reduces glial cyst and improves functional outcome after spinal cord compression,” World Neurosurgery, vol. 81, no. 1, pp. 183–190, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. R. Quertainmont, D. Cantinieaux, O. Botman, S. Sid, J. Schoenen, and R. Franzen, “Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions,” PLoS ONE, vol. 7, no. 6, Article ID e39500, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Koda, T. Kamada, M. Hashimoto et al., “Adenovirus vector-mediated ex vivo gene transfer of brain-derived neurotrophic factor to bone marrow stromal cells promotes axonal regeneration after transplantation in completely transected adult rat spinal cord,” European Spine Journal, vol. 16, no. 12, pp. 2206–2214, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. J. E. Springer, R. D. Azbill, and P. E. Knapp, “Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury,” Nature Medicine, vol. 5, no. 8, pp. 943–946, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Warden, N. I. Bamber, H. Li et al., “Delayed glial cell death following wallerian degeneration in white matter tracts after spinal cord dorsal column cordotomy in adult rats,” Experimental Neurology, vol. 168, no. 2, pp. 213–224, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. S. M. Lee, T. Y. Yune, S. J. Kim et al., “Minocycline reduces cell death and improves functional recovery after traumatic spinal cord injury in the rat,” Journal of Neurotrauma, vol. 20, no. 10, pp. 1017–1027, 2003. View at Publisher · View at Google Scholar · View at Scopus
  17. S. A. Nottingham and J. E. Springer, “Temporal and spatial distribution of activated caspase-3 after subdural kainic acid infusions in rat spinal cord,” Journal of Comparative Neurology, vol. 464, no. 4, pp. 463–471, 2003. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Casha, W. R. Yu, and M. G. Fehlings, “Oligodendroglial apoptosis occurs along degenerating axons and is associated with FAS and p75 expression following spinal cord injury in the rat,” Neuroscience, vol. 103, no. 1, pp. 203–218, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. Y. Wang, Z. Sun, K. Zhang, G. Xu, and G. Li, “Bcl-2 in suppressing neuronal apoptosis after spinal cord injury,” World Journal of Emergency Medicine, vol. 2, no. 1, pp. 38–44, 2011. View at Google Scholar
  20. R. R. Kotipatruni, V. R. Dasari, K. K. Veeravalli, D. H. Dinh, D. Fassett, and J. S. Rao, “P53- and bax-mediated apoptosis in injured rat spinal cord,” Neurochemical Research, vol. 36, no. 11, pp. 2063–2074, 2011. View at Publisher · View at Google Scholar · View at Scopus
  21. J. K. Lee, H. K. Jin, and J.-S. Bae, “Bone marrow-derived mesenchymal stem cells attenuate amyloid β-induced memory impairment and apoptosis by inhibiting neuronal cell death,” Current Alzheimer Research, vol. 7, no. 6, pp. 540–548, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. F. Yin, L. Guo, C.-Y. Meng et al., “Transplantation of mesenchymal stem cells exerts anti-apoptotic effects in adult rats after spinal cord ischemia-reperfusion injury,” Brain Research, vol. 1561, pp. 1–10, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Wang, X.-J. He, Q. Li, H.-P. Li, and D. Wang, “In vitro culture of human fetal olfactory bulb olfactory ensheathing cells by three purification methods,” Journal of Clinical Rehabilitative Tissue Engineering Research, vol. 12, no. 16, pp. 3089–3091, 2008. View at Google Scholar · View at Scopus
  24. H. H. Nash, R. C. Borke, and J. J. Anders, “New method of purification for establishing primary cultures of ensheathing cells fom the adult olfactory bulb,” Glia, vol. 34, no. 2, pp. 81–87, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. W. Qian, Y. Na, J. Yufeng et al., “Culture and biologic characteristics identification of bone marrow stromal cells in rats,” Progress in Modern Biomedicine, vol. 10, no. 8, pp. 1473–1476, 2010. View at Google Scholar
  26. D. M. Basso, M. S. Beattie, and J. C. Bresnahan, “A sensitive and reliable locomotor rating scale for open field testing in rats,” Journal of Neurotrauma, vol. 12, no. 1, pp. 1–21, 1995. View at Publisher · View at Google Scholar · View at Scopus
  27. E. Syková, P. Jendelová, L. Urdzíková, P. Lesný, and A. Hejčl, “Bone marrow stem cells and polymer hydrogels—two strategies for spinal cord injury repair,” Cellular and Molecular Neurobiology, vol. 26, no. 7-8, pp. 1113–1129, 2006. View at Publisher · View at Google Scholar
  28. V. Sahni and J. A. Kessler, “Stem cell therapies for spinal cord injury,” Nature Reviews Neurology, vol. 6, no. 7, pp. 363–372, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Hernández, A. Torres-Espín, and X. Navarro, “Adult stem cell transplants for spinal cord injury repair: current state in preclinical research,” Current Stem Cell Research and Therapy, vol. 6, no. 3, pp. 273–287, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. A. J. Mothe and C. H. Tator, “Advances in stem cell therapy for spinal cord injury,” The Journal of Clinical Investigation, vol. 122, no. 11, pp. 3824–3834, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. D. P. Ankeny, D. M. McTigue, and L. B. Jakeman, “Bone marrow transplants provide tissue protection and directional guidance for axons after contusive spinal cord injury in rats,” Experimental Neurology, vol. 190, no. 1, pp. 17–31, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Lee, S. Kuroda, H. Shichinohe et al., “Migration and differentiation of nuclear fluorescence-labeled bone marrow stromal cells after transplantation into cerebral infarct and spinal cord injury in mice,” Neuropathology, vol. 23, no. 3, pp. 169–180, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. Y.-B. Deng, X.-G. Liu, Z.-G. Liu, X.-L. Liu, Y. Liu, and G.-Q. Zhou, “Implantation of BM mesenchymal stem cells into injured spinal cord elicits de novo neurogenesis and functional recovery: evidence from a study in rhesus monkeys,” Cytotherapy, vol. 8, no. 3, pp. 210–214, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. Y. B. Deng, Y. Liu, W. B. Zhu et al., “The co-transplantation of human bone marrow stromal cells and embryo olfactory ensheathing cells as a new approach to treat spinal cord injury in a rat model,” Cytotherapy, vol. 10, no. 6, pp. 551–564, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. G. L. Li, G. Brodin, M. Farooque et al., “Apoptosis and expression of Bcl-2 after compression trauma to rat spinal cord,” Journal of Neuropathology and Experimental Neurology, vol. 55, no. 3, pp. 280–289, 1996. View at Publisher · View at Google Scholar · View at Scopus
  36. B. A. Citron, P. M. Arnold, C. Sebastian et al., “Rapid upregulation of caspase-3 in rat spinal cord after injury: mRNA, protein, and cellular localization correlates with apoptotic cell death,” Experimental Neurology, vol. 166, no. 2, pp. 213–226, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. S.-U. Kuh, Y.-E. Cho, D.-H. Yoon, K.-N. Kim, and Y. Ha, “Functional recovery after human umbilical cord blood cells transplantation with brain-derived neutrophic factor into the spinal cord injured rat,” Acta Neurochirurgica, vol. 147, no. 9, pp. 985–992, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. Liu, Y. Qu, T. J. Stewart et al., “Embryonic stem cells differentiate into oligodendrocytes and myelinate in culture and after spinal cord transplantation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 11, pp. 6126–6131, 2000. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Lu, L. L. Jones, and M. H. Tuszynski, “BDNF-expressing marrow stromal cells support extensive axonal growth at sites of spinal cord injury,” Experimental Neurology, vol. 191, no. 2, pp. 344–360, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Lu, L. L. Jones, E. Y. Snyder, and M. H. Tuszynski, “Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury,” Experimental Neurology, vol. 181, no. 2, pp. 115–129, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Saporta, J.-J. Kim, A. E. Willing, E. S. Fu, C. D. Davis, and P. R. Sanberg, “Human umbilical cord blood stem cells infusion in spinal cord injury: engraftment and beneficial influence on behavior,” Journal of Hematotherapy and Stem Cell Research, vol. 12, no. 3, pp. 271–278, 2003. View at Publisher · View at Google Scholar · View at Scopus