Acute Transplantation of Human Olfactory Mucosa-Derived Olfactory Ensheathing Cells Fails to Improve Locomotor Recovery in Rats
-
Mina Afhami
,
Mansoureh Hashemi
,
Khashayar Afshari
,
Jamal Chenari
,
Seyed Mohammad Tavangar
,
Mahmoudreza Hadjighassem
,
Ahmad Reza Dehpour
,
Ahad Muhammadnejad
,
Arvin Haj-Mirzaian
,
Vafa Rahimi-Movaghar
Abstract
Olfactory ensheathing cells-based therapy for spinal cord injury (SCI) repair has been a possible treatment for clinical study because of their safety in autologous transplantation and potential regenerative capability. However, there are contradictory reports on the results after transplantation in animal models. The purpose of this research was to investigate the effect of acute transplantation of human mucosa-derived olfactory ensheathing cells (OECs) on the repair of the spinal cord. Human olfactory ensheathing cells were isolated from the human mucosa and cultured under supplemented neuronal cell culture medium. They were characterized by immunocytochemistry for olfactory ensheathing cell markers. We induced spinal cord injury at T8-T9 of rats by aneurysm clips and simultaneously injected two million OECs into subarachnoid space of spinal cord. Sensory and motor behaviors were recorded by tail-flick reflex (TFR) and BBB scores, respectively every week for seven weeks after injury. Morphology and S100-beta antigen expression in olfactory ensheathing cells of the human olfactory mucosa was confirmed by immunostaining. OECs transplantation did not recover inflammation, neuronal vacuolation, hemorrhage, and cyst formation. These findings suggest that OECs transplantation in this experimental setting did not lead to tissue regeneration to enhance locomotion. These results broaden current knowledge and are additions to the science and literature.
Kato T, Honmou O, Uede T, Hashi K, Kocsis JD. Transplantation of human olfactory ensheathing cells elicits remyelination of demyelinated rat spinal cord. Glia 2000; 30(3): 209-218.
Einstein O, Ben-Hur T. The changing face of neural stem cell therapy in neurologic diseases. Arch Neurol 2008; 65(4): 452-456.
McDonald JW, Becker D, Holekamp TF, Howard M, Liu S, Lu A, et al. Repair of the injured spinal cord and the potential of embryonic stem cell transplantation. J Neurotrauma 2004; 21(4):383-393.
Vaquero J, Zurita M. Bone marrow stromal cells for spinal cord repair: a challenge for contemporary neurobiology. Histol Histopathol 2009; 24(1):107-116.
Lakatos A, Franklin RJ, Barnett SC. Olfactory ensheathing cells and Schwann cells differ in their in vitro interactions with astrocytes. Glia 2000; 32(3):214-225.
Li J, Lepski G. Cell transplantation for spinal cord injury: a systematic review. Biomed Res Int 2013; 2013:7864-7875.
Mackay-Sim A, Feron F, Cochrane J, Bassingthwaighte L, Bayliss C, Davies W, et al. Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 2008; 131(Pt 9):2376-2386.
Vincent AJ, West AK, Chuah MI. Morphological and functional plasticity of olfactory ensheathing cells. J Neurocytol 2005; 34(1-2):65-80.
Pastrana E, Moreno-Flores MT, Avila J, Wandosell F, Minichiello L, Diaz-Nido J. BDNF production by olfactory ensheathing cells contributes to axonal regeneration of cultured adult CNS neurons. Neurochem Int 2007; 50(3): 491-498.
Raisman G, Carlstedt T, Choi D, Li Y. Clinical prospects for transplantation of OECs in the repair of brachial and lumbosacral plexus injuries: opening a door. Exp Neurol 2011; 229(1): 168-173.
Plant GW, Currier PF, Cuervo EP, Bates ML, Pressman Y, Bunge MB, et al. Purified adult ensheathing glia fail to myelinate axons under culture conditions that enable Schwann cells to form myelin. J Neurosci 2002; 22(14): 6083-6091.
Au E, Richter MW, Vincent AJ, Tetzlaff W, Aebersold R, Sage EH, et al. SPARC from olfactory ensheathing cells stimulates Schwann cells to promote neurite outgrowth and enhances spinal cord repair. J Neurosci 2007; 27(27):7208-7221.
Hashemi M, Fallah A, Aghayan HR, Arjmand B, Yazdani N, Verdi J, et al. A New Approach in Gene Therapy of Glioblastoma Multiforme: Human Olfactory Ensheathing Cells as a Novel Carrier for Suicide Gene Delivery. Mol Neurobiol 2016; 53(8): 5118-5128.
Rahimi-Movaghar V, Yazdi A, Mohammadi M. Usefulness of the tail-flick reflex in the prognosis of functional recovery in paraplegic rats. Surg Neurol 2008; 70(3):323-325.
Basso DM, Beattie MS, Bresnahan JC. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 1995; 12(1):1-21.
Zakeri M, Afshari K, Gharedaghi MH, Shahsiah R, Rahimian R, Maleki F, et al. Lithium protects against spinal cord injury in rats: role of nitric oxide. J Neurol Surg A Cent Eur Neurosurg 2014; 75(6): 427-433.
Qiao F, Atkinson C, Kindy MS, Shunmugavel A, Morgan BP, Song H, et al. The alternative and terminal pathways of complement mediate post-traumatic spinal cord inflammation and injury. Am J Pathol 2010; 177(6):3061-3070.
Nategh M, Firouzi M, Naji-Tehrani M, Oryadi Zanjani L, Hassannejad Z, Nabian MH, et al.Subarachnoid Space Transplantation of Schwann and/or Olfactory Ensheathing Cells Following Severe Spinal Cord Injury Fails to Improve Locomotor Recovery in Rats. Acta Med Iran 2016; 54(9):562-569.
Okano H, Ogawa Y, Nakamura M, Kaneko S, Iwanami A, Toyama Y. Transplantation of neural stem cells into the spinal cord after injury. Semin Cell Dev Biol 2003; 14(3):191-198.
Collazos-Castro JE, Muñetón-Gómez VC, Nieto-Sampedro M. Olfactory glia transplantation into cervical spinal cord contusion injuries. Journal of Neurosurgery: Spine 2005; 3(4):308-317.
Keyvan-Fouladi N, Raisman G, Li Y. Functional repair of the corticospinal tract by delayed transplantation of olfactory ensheathing cells in adult rats. J Neurosci 2003; 23(28):9428-9434.
Toft A, Scott DT, Barnett SC, Riddell JS. Electrophysiological evidence that olfactory cell transplants improve function after spinal cord injury. Brain 2007; 130(4):970-984.
Ramón-Cueto A, Cordero MI, Santos-Benito FF, Avila J. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000; 25(2):425-435.
Wu S, Cui G, Shao H, Du Z, Ng JC, Peng C. The Cotransplantation of Olfactory Ensheathing Cells with Bone Marrow Mesenchymal Stem Cells Exerts Antiapoptotic Effects in Adult Rats after Spinal Cord Injury. Stem Cells Int 2015; 2015: 1-13.
Yamamoto M, Raisman G, Li D, Li Y. Transplanted olfactory mucosal cells restore paw reaching function without regeneration of severed corticospinal tract fibres across the lesion. Brain Res 2009; 1303:26-31.
Takami T, Oudega M, Bates ML, Wood PM, Kleitman N, Bunge MB.Schwann cell but not olfactory ensheathing glia transplants improve hindlimb locomotor performance in the moderately contused adult rat thoracic spinal cord. Journal of Neuroscience 2002; 22(15):6670-6681.
Plant GW, Christensen CL, Oudega M, Bunge MB. Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. Journal of neurotrauma 2003; 20(1):1-16.
Lopez-Vales R, Fores J, Verdu E, Navarro X. Acute and delayed transplantation of olfactory ensheathing cells promote partial recovery after complete transection of the spinal cord. Neurobiol Dis 2006; 21(1):57-68.
Fouad K, Pearson K. Restoring walking after spinal cord injury. Progress in neurobiology 2004; 73(2):107-126.
Kocsis JD, Lankford KL, Sasaki M, Radtke C. Unique in vivo properties of olfactory ensheathing cells that may contribute to neural repair and protection following spinal cord injury. Neuroscience letters 2009; 456(3):137-142.
Lipson AC, Widenfalk J, Lindqvist E, Ebendal T, Olson L. Neurotrophic properties of olfactory ensheathing glia. Experimental neurology 2003; 180(2):167-171.
Barnett SC, Riddell JS. Olfactory ensheathing cell transplantation as a strategy for spinal cord repair—what can it achieve? Nature clinical practice Neurology 2007; 3(3):152-161.
| Files | ||
| Issue | Vol 56, No 7 (2018) | |
| Section | Original Article(s) | |
| Keywords | ||
| Spinal cord injury Olfactory ensheathing cells Functional recovery Rat | ||
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