Delayed Xenograft Transplantation of Mouse Olfactory Ensheathing Cells in Adult Rats

Maryam Naghynajadfard

Abstract


Regeneration of the central nervous system after injury using appropriate cells for transplantation is a controversial issue. Accessibility of allograft olfactory ensheathing cells to transplant in the spinal cord of patients is not applicable. Therefore, in this study, an attempt has been made to xenotransplant cells from mouse into a corticospinal tract lesion in a rat in order to achieve a plausible preclinical approach for future application to a clinical study. Adult rats were trained to use their forepaws for retrieving. The dorsal corticospinal tract was lesioned by a stereotactic radio-frequency lesion maker at the level of the first/second cervical segments. Rats that had shown no forepaw retrieval by 8 weeks were xenotransplanted with a suspension of cultured olfactory ensheathing cells derived from the mouse olfactory bulb. Starting between 1 and 3 weeks, 10 rats with transplants bridging the lesion site resumed ipsilateral forepaw reaching. After transplanting cells into the lesion side, the cross and horizontal sections of GFAP and NF staining of 10 animals that have the Directed Forepaw Reaching (DFR) function returned showed the regenerated CST fibers in the lesion area after 8 weeks postoperative. Xenotrasplant of olfactory ensheathing cells from the mouse olfactory bulb into a rat corticospinal tract lesion was promising and positive. Animals that had difficulty in Directed Forepaw Reaching had returned the function 8 weeks postoperatively.

 

Doi: 10.28991/SciMedJ-2022-04-02-01

Full Text: PDF


Keywords


Xenograft; Olfactory Ensheating Cells; Transplantation; Corticospinal Tract; Repair; Rat.

References


Delarue, Q., & Guérout, N. (2022). Transplantation of Olfactory Ensheathing Cells: Properties and Therapeutic Effects after Transplantation into the Lesioned Nervous System. Neuroglia, 3(1), 1–22. doi:10.3390/neuroglia3010001.

Chuah, M. I., & Au, C. (1991). Olfactory Schwann cells are derived from precursor cells in the olfactory epithelium. Journal of Neuroscience Research, 29(2), 172–180. doi:10.1002/jnr.490290206.

Huard, J. M. T., Youngentob, S. L., Goldstein, B. J., Luskin, M. B., & Schwob, J. E. (1998). Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. Journal of Comparative Neurology, 400(4), 469–486. doi:10.1002/(SICI)1096-9861(19981102)400:4<469::AID-CNE3>3.0.CO;2-8.

Lu, J., & Ashwell, K. (2002). Olfactory ensheathing cells: Their potential use for repairing the injured spinal cord. Spine, 27(8), 887–892. doi:10.1097/00007632-200204150-00021.

Li, Y., Li, D., & Raisman, G. (2005). Interaction of olfactory ensheathing cells with astrocytes may be the key to repair of tract injuries in the spinal cord: The “pathway hypothesis.” Journal of Neurocytology, 34(3–5), 343–351. doi:10.1007/s11068-005-8361-1.

Reshamwala, R., Shah, M., St John, J., & Ekberg, J. (2019). Survival and Integration of Transplanted Olfactory Ensheathing Cells are Crucial for Spinal Cord Injury Repair: Insights from the Last 10 Years of Animal Model Studies. Cell Transplantation, 28(1_suppl), 132S-159S. doi:10.1177/0963689719883823.

Nakhjavan-Shahraki, B., Yousefifard, M., Rahimi-Movaghar, V., Baikpour, M., Nasirinezhad, F., Safari, S., Yaseri, M., Moghadas Jafari, A., Ghelichkhani, P., Tafakhori, A., & Hosseini, M. (2018). Transplantation of olfactory ensheathing cells on functional recovery and neuropathic pain after spinal cord injury; Systematic review and meta-analysis. Scientific Reports, 8(1), 325. doi:10.1038/s41598-017-18754-4.

Wu, A., Lauschke, J. L., Morris, R., & Waite, P. M. E. (2009). Characterization of rat forepaw function in two models of cervical dorsal root injury. Journal of Neurotrauma, 26(1), 17–29. doi:10.1089/neu.2008.0675.

Gibney, S. M., & McDermott, K. W. (2009). Sonic hedgehog promotes the generation of myelin proteins by transplanted oligosphere-derived cells. Journal of Neuroscience Research, 87(14), 3067–3075. doi:10.1002/jnr.22138.

Yamamoto, M., Raisman, G., Li, D., & Li, Y. (2009). Transplanted olfactory mucosal cells restore paw reaching function without regeneration of severed corticospinal tract fibres across the lesion. Brain Research, 1303, 26–31. doi:10.1016/j.brainres.2009.09.073.

Li, Y., & Raisman, G. (1995). Sprouts from Cut Corticospinal Axons Persist in the Presence of Astrocytic Scarring in Long-Term Lesions of the Adult Rat Spinal Cord. Experimental Neurology, 134(1), 102–111. doi:10.1006/exnr.1995.1041.

Emmett, C. J., Jaques-Berg, W., & Seeley, P. J. (1990). Microtransplantation of neural cells into adult rat brain. Neuroscience, 38(1), 213–222. doi:10.1016/0306-4522(90)90387-J.

Keyvan-Fouladi, N., Raisman, G., & Li, Y. (2003). Functional Repair of the Corticospinal Tract by Delayed Transplantation of Olfactory Ensheathing Cells in Adult Rats. Journal of Neuroscience, 23(28), 9428–9434. doi:10.1523/jneurosci.23-28-09428.2003.

Trinh, V. T., Fahim, D. K., Shah, K., Tummala, S., McCutcheon, I. E., Sawaya, R., Suki, D., & Prabhu, S. S. (2013). Subcortical injury is an independent predictor of worsening neurological deficits following awake craniotomy procedures. Neurosurgery, 72(2), 160–169. doi:10.1227/NEU.0b013e31827b9a11.

Watanabe, K., Kondo, K., Yamasoba, T., & Kaga, K. (2007). Age-related change in the axonal diameter of the olfactory nerve in mouse lamina propria. Acta Oto-Laryngologica, 127(SUPPL. 559), 108–112. doi:10.1080/03655230701597598.

Whishaw, I. Q., & Pellis, S. M. (1990). The structure of skilled forelimb reaching in the rat: A proximally driven movement with a single distal rotatory component. Behavioural Brain Research, 41(1), 49–59. doi:10.1016/0166-4328(90)90053-h.

Americam spinal injury association Net. Available online: https://asia-spinalinjury.org/learning/ (accessed on January 2022).

Imaizumi, T., Lankford, K. L., Burton, W. V., Fodor, W. L., & Kocsis, J. D. (2000). Xenotransplantation of transgenic pig olfactory ensheathing cells promotes axonal regeneration in rat spinal cord. Nature Biotechnology, 18(9), 949–953. doi:10.1038/79432.

Yu, Y., Li, L., Lin, S., & Hu, J. (2022). Update of application of olfactory ensheathing cells and stem cells/exosomes in the treatment of retinal disorders. Stem Cell Research and Therapy, 13(1), 11. doi:10.1186/s13287-021-02685-z.

Zhang, L., Zhuang, X., Kotitalo, P., Keller, T., Krzyczmonik, A., Haaparanta-Solin, M., Solin, O., Forsback, S., Grönroos, T. J., Han, C., López-Picón, F. R., & Xia, H. (2021). Intravenous transplantation of olfactory ensheathing cells reduces neuroinflammation after spinal cord injury via interleukin-1 receptor antagonist. Theranostics, 11(3), 1147–1161. doi:10.7150/thno.52197.

Plant, G. W., Christensen, C. L., Oudega, M., & Bunge, M. B. (2003). Delayed transplantation of olfactory ensheathing glia promotes sparing/regeneration of supraspinal axons in the contused adult rat spinal cord. Journal of Neurotrauma, 20(1), 1–16. doi:10.1089/08977150360517146.

McKeon, R. J., Höke, A., & Silver, J. (1995). Injury-induced proteoglycans inhibit the potential for laminin-mediated axon growth on astrocytic scars. Experimental Neurology, 136(1), 32–43. doi:10.1006/exnr.1995.1081.

Choi, D., & Raisman, G. (2003). Immune rejection of a facial nerve xenograft does not prevent regeneration and the return of function: An experimental study. Neuroscience, 121(2), 501–507. doi:10.1016/S0306-4522(03)00433-0.

Cendales, L. C., Kanitakis, J., Schneeberger, S., Burns, C., Ruiz, P., Landin, L., Remmelink, M., Hewitt, C. W., Landgren, T., Lyons, B., Drachenberg, C. B., Solez, K., Kirk, A. D., Kleiner, D. E., & Racusen, L. (2008). The Banff 2007 working classification of skin-containing composite tissue allograft pathology. American Journal of Transplantation, 8(7), 1396–1400. doi:10.1111/j.1600-6143.2008.02243.x.

de Groen, P. C. (1989). Cyclosporine: A Review and Its Specific Use in Liver Transplantation. Mayo Clinic Proceedings, 64(6), 680–689. doi:10.1016/S0025-6196(12)65348-8.

Miach, P. J. (1986). Cyclosporin A in organ transplantation. Medical Journal of Australia, 145(3–4), 146–150. doi:10.5694/j.1326-5377.1986.tb113775.x.

Murohara, T., Ikeda, H., Duan, J., Shintani, S., Sasaki, K. I., Eguchi, H., Onitsuka, I., Matsui, K., & Imaizumi, T. (2000). Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. Journal of Clinical Investigation, 105(11), 1527–1536. doi:10.1172/JCI8296.


Full Text: PDF

DOI: 10.28991/SciMedJ-2022-04-02-01

Refbacks

  • There are currently no refbacks.


Copyright (c) 2023 Maryam Naghynajadfard