The Effect of Transglutaminase on the Recovery of Somatosensory Evoked Potentials in the Rat Model of Spinal Cord Injury

백서 척수손상 모델에서 체성감각유발전위의 회복에 대한 트랜스글루타미네이즈 효과

Lee, Ho-Yeon;Kwun, Byung-Duk;Kim, Soo-Youl
이호연;권병덕;김수열

  • Published : 20030800

Abstract

Objective : The authors present an investigation of the effect of transglutaminase(TG) on the recovery of somatosensory evoked potentials in the rat model of spinal cord injury. Methods : Female Sprague-Dawley rats (280-310g) were used for this study. Rats were divided into two groups : TG treated and control. The lesion was made by transecting the right dorsal column of the thoracic spinal cord without damage to the vasculature using specially devised micro-glass pipette after laminectomy. For TG treated group, normal saline with TG were injected into the lesion site using micro-pipette through the opening of the dura. Saltatory repetitive somatosensory evoked potentials(SSEPs) recording were carried out on post-injury 6th and 12th week. Results : The amplitudes of N19 were 1.28$\pm$1.60$\mu$V on 6th week, 3.45$\pm$3.63$\mu$V on 12th week in control group(n=10) and 1.46$\pm$1.75$\mu$V on 6th week and 5.01$\pm$2.65$\mu$V on 12th week in TG-treated group(n=11). Statistically significant recovery of SSEPs were seen in TG-treated group(p=0.003, Wilcoxon Signed Ranks Test). In TGtreated group, vacuolated degeneration around the lesion site was rarely observed on histological evaluation. Conclusion : This study demonstrates the possibility of long-term survival and saltatory recording of SSEPs in small animals like rats, after selective spinal cord injury. In addition, this study shows that TG is a factor facilitating the recovery of injured axon of central nervous system.

Keywords

References

  1. Allen AR : Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column. A preliminary report. JAMA 57 : 878-880, 1911
  2. Anderson DK, Means ED, Walters TR : Spinal cord energy metabolism in normal and postlaminectomy cats. J Neurosurg 52 : 387-391, 1980 https://doi.org/10.3171/jns.1980.52.3.0387
  3. Andersson SA, Norrsell K, Norrsell U : Spinal pathways projecting to the cerebral first somatosensory area in the monkey. J Physiol 225 : 589-597, 1972
  4. Bennett MH, McCallum JE, Stasiak TS : The effect of dorsal spinal cord infarction on the somatosensory evoked response in cats. Proc Soc Neurosci : 696, 1975
  5. Bernstein JJ, Goldberg WJ : Experimental spinal cord transplantation as a mechanism of spinal cord regeneration (Review). Paraplegia 33 : 250-253, 1995 https://doi.org/10.1038/sc.1995.57
  6. Bregman BS, Broude E, McAtee M, Kelley MS : Transplants and neurotrophic factors prevent atrophy of mature CNS neurons after spinal cord injury. Exp Neurol 149 : 13-27, 1998 https://doi.org/10.1006/exnr.1997.6669
  7. Bregman BS, McAtee M, Dai HN, Kuhn PL : Neurotrophic factors increase axonal growth after spinal cord injury and transplantation in the adult rat. Exp Neurol 148 : 475-494, 1997 https://doi.org/10.1006/exnr.1997.6705
  8. Brown AG, Kirk EJ : Ipsilateral and contralateral inhibitory actions on transmission through the spinocervical tract. Brain Res 43 : 268-271, 1972 https://doi.org/10.1016/0006-8993(72)90294-6
  9. Campbell JB, DeCrescito V, Tomasula JJ, Demopoulos HB, Flamm ES, Ransohoff J : Experimental treatment of spinal cord contusion in the cat. Surg Neurol 1 : 102-106, 1973
  10. Cusick JF, Myklebust JB, Larson SJ, Sances A Jr : Spinal evoked potentials in the primate: neural substrate. J Neurosurg 49 : 551-557, 1978 https://doi.org/10.3171/jns.1978.49.4.0551
  11. Davis GR, Mcclellan AD : Extent and time course of restoration of descending brainstem projections in spinal cord-transected lamprey. J Comp Neurol 344 : 65-82. 1994 https://doi.org/10.1002/cne.903440106
  12. Dolan EJ, Transfeldt EE, Tator CH, Simmons EH, Hughes KF : The effect of spinal distraction on regional spinal cord blood flow in cats. J Neurosurg 53 : 756-764, 1980 https://doi.org/10.3171/jns.1980.53.6.0756
  13. Eitan S, Zisling R, Cohen A, Belkin M, Hirschberg DL, Lotan M, et al : Identification of an interleukin 2-like substance as a factorcyto-toxic to oligodendrocytes and associated with central nervous system regeneration. Proc Natl Acad Sci USA 89 : 5442-5446, 1992 https://doi.org/10.1073/pnas.89.12.5442
  14. Eitan S, Schwartz M : A transglutaminase that converts interleukin-2 into a factor cytotoxic to oligodendrocytes. Science 261 : 106-108 1993 https://doi.org/10.1126/science.8100369
  15. Eitan S, Solomon A, Lavie V, Yoles E, Hirschberg DL, Belkin M, et al : Recovery of visual response of injured adult rat optic nerves treated with transglutaminase. Science 264 : 1764-1768, 1994 https://doi.org/10.1126/science.7911602
  16. Fehlings MG, Tator CH, Linden RD, Piper IR : Motor and somatosensory evoked potentials recorded from the rat. Electroencephalogr Clin Neurophysiol 69 : 65-78, 1988 https://doi.org/10.1016/0013-4694(88)90036-3
  17. Feraboli-Lohnherr D, Orsal D, Yakovleff A, Gimenez Y, Ribotta M, Privat A : Recovery of iocomotor activity in the adult chronic spinal rat after sublesional transplantation of embryonic nervous cells: specific role of serotonergic neurons. Exp Brain Res 113 : 443-453, 1997 https://doi.org/10.1007/PL00005597
  18. Gaze RM, Gordon G : Some observations on the central pathway for cutaneous impulses in the cat. Q J Exp Physiol 40 : 187-194, 1955
  19. Grill R, Murai K, Blesch A, Gage FH, Tuszynski MH : Cellular delivery of neurotrophin-3 promotes corticospinal axonal growth and partial functional recovery after spinal cord injury. J Neurosci 17 : 5560-5572, 1997
  20. Herdegen T, Skene P, Bahr M : The c-Jun transcription factorbipotential mediator of neuronal death, survival and regeneration. Trends Neurosci 20 : 227-231, 1997 https://doi.org/10.1016/S0166-2236(96)01000-4
  21. Houle JD, Ye JH, Kane CJM : Axonal regeneration by chronically injured supraspinal neurons can be enhanced by esposure to insulin-like growth factor, basic fibroblast growth factor or transforming growth factor beta. Restorative Neurol Neurosci 10 : 205-215, 1997
  22. Houle JD, Ye JH : Changes occur in the ability to promote axonal regeneration as the post-injury period increases. Neuroreport 8 : 751-755, 1997
  23. Houle JD, Skinner RD, Garcia-Rill E, Turner KL : Synaptic evoked potentials from regenerating dorsal root axons within fetal spinal cord tissue transplants. Exp Neurol 139 : 278-990, 1996 https://doi.org/10.1006/exnr.1996.0101
  24. Hurlbert RJ, Koyanagi I, Tator CH:Sensory evoked potentials for selective monitoring of the rat spinal cord : A cerebellar evoked potential to assess ventral cord integrity. J Neurotrauma 10 : 181-200, 1993 https://doi.org/10.1089/neu.1993.10.181
  25. Itoh Y, Tessler A, Kowada M, Pinter M : Electrophysiological responses in foetal spinal cord transplants evoked by regenerated dorsal root axons. Acta Neurochir Suppl 58 : 24-26, 1993
  26. Kobayashi NR, Fan DP, Giehl KM, Bedard AM, Wiegand SJ, Tetz-laff W : BDNF and NT-4/5 prevent atrophy of rat rubrospinal neurons after cervical axotomy, stimulate GAP-43 and Ta1-tubulin mRNA expression, and promote axonal regeneration. J Neurosci 17 : 9583-9595, 1997
  27. Mark RF, Steiner J : Cortical projection of impulses in myelinated cutaneous afferent nerve fibres of the cat. J Physiol 142 : 544-562, 1958
  28. Morin F : A new spinal pathway for cutaneous impulses. Am J Physiol 183 : 245-252, 1955
  29. Nockels R, Young W : Pharmacologic strategies in the treatment of experimental spinal cord injury. J Neurotrauma 9 (Suppl) : S211-S217, 1992
  30. Oudega M, Hagg T : Nerve growth factor promotes regeneration of sensory axons into adult rat spinal cord. Exp Neurol 140 : 218-229, 1996 https://doi.org/10.1006/exnr.1996.0131
  31. Oudega M, Varon S, Hagg T : Regeneration of adult rat sensory axons into intraspinal nerve grafts : promoting effects of conditioning lesion and graft predegeneration. Exp Neurol 129 : 194-206, 1994 https://doi.org/10.1006/exnr.1994.1161
  32. Powers SK, Bolger CA, Edwards MS : Spinal cord pathways mediating somatosensory evoked potentials. J Neurosurg 57 : 472-482, 1982 https://doi.org/10.3171/jns.1982.57.4.0472
  33. Rabchevsky AG, Streit WJ : Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J Neurosci Res 47 : 34-48, 1997 https://doi.org/10.1002/(SICI)1097-4547(19970101)47:1<34::AID-JNR4>3.0.CO;2-G
  34. Rivlin AS, Tator CH : Effects of duration of acute spinal cord compression in a new acute cord injury model in the rat. Surg Neurol 10 : 39-43, 1978
  35. Sandler AN, Tator CH : Review of the effect of spinal cord trauma on the vessels and blood flow in the spinal cord. J Neurosurg 45 : 638-646 1976 https://doi.org/10.3171/jns.1976.45.6.0638
  36. Vidal-Sanz, M, Bray GM, Villegas-Perez MP, Thanos S, Aguayo AJ : Axonal regeneration and synapse formation in the superior colliculus by retinal ganglion cells in the adult rat. J Neurosci 7 : 2894-2909, 1987
  37. Watson BD, Dietrich WD, Busto R : Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann Neurol 17 : 497-504, 1985 https://doi.org/10.1002/ana.410170513
  38. Xu XM, Guenard V, Kleitman N, Aebischer P, Bunge MB : A combination of BDNF and NT-3 promotes supraspinal axonal regeneration into Schwann cell grafts in adult rat thoracic spinal cord. Exp Neurol 134 : 261-272, 1995 https://doi.org/10.1006/exnr.1995.1056
  39. Xu XM, Guenard V, Kleitman N, Bunge MB : Axonal regeneration into Schwann cell-seeded guidance channels grafted into transected adult rat spinal cord. J Comp Neurol 351 : 145-160, 1994
  40. Ye JH, Houle JD : Treatment of the chronically injured spinal cord with neurotrophic factors can promote axonal regeneration from supraspinal neurons. Exp Neurol 143 : 70-81, 1997 https://doi.org/10.1006/exnr.1996.6353
  41. Zammit PS, Clarke JD, Golding JP, Goodbrand IA, Tonge DA : Macrophage response during axonal regeneration in the axolotl central and peripheral nervous system. Neuroscience 54 : 781-789, 1993 https://doi.org/10.1016/0306-4522(93)90247-D