Cell and Organ Transplantology. 2017; 5(1):87-93.
DOI: 10.22494/COT.V5I1.71
In vivo and in vitro models of traumatic injuries of the spinal cord
Rybachuk O. A.1,2, Arkhypchuk I. V.1,3, Lazarenko Yu. A.1,4
1Bogomoletz Institute of Physiology NAS of Ukraine, Kyiv, Ukraine
2State Institute of Genetic and Regenerative Medicine NAMS, Kyiv, Ukraine
3Educational and Scientific Center “Institute of Biology and Medicine“ Taras Shevchenko National University, Kyiv, Ukraine
4National University “Kyiv-Mohyla Academy”, Kyiv, Ukraine
Abstract
In recent years, there is a growing interest in the mechanisms of regeneration of damaged nerve tissue, including the spinal cord, as its injuries are quite common due to traffic accidents, industrial injuries and military actions. Damage to the spinal cord results in the loss of functional activity of the body below the injury site, which affects person’s ability to self-service and significantly reduces its efficiency. The effects of spinal injuries annually cause significant social and economic losses worldwide, including Ukraine. The development of new treatments for pathologies of the central nervous system requires mandatory pre-testing of their effectiveness in experiments in vitro and in vivo. Therefore, searching and creation of optimal animal model of spinal cord injury is in order to it meets most complete picture of the damage characteristic of real conditions in humans. This is an important task of modern neurophysiology. Such models can be used, primarily, for a more detailed clarification of the pathogenesis of all levels of nerve tissue damage and research of its own recovery potential by endogenous reparation mechanisms. In addition, experimental models allow to estimate the safety and predict the effectiveness of various therapeutic approaches to spinal cord injury.
Key words: spinal cord injury; neural tissue injury modelling; glial scar; regeneration
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| 1. Holovatsky AS, Cherkasov V, Sapin MR, et al. Anatomіja ljudini u tr’oh tomah [Human Anatomy in three volumes]. Vinnitsa: Nova Kniga – Vinnitsa: New Book, 2007. 456 p. [In Ukrainian]. | ||||
| 2. Marunenko IM, Nevedomska YO, Volkovska GI. Anatomіja, fіzіologіja, evoljucіja nervovoї sistemi [Anatomy, physiology, evolution of the nervous system]. Kiїv: «Centr uchbovoї lіteraturi» – Кyiv: “Center of educational literature”, 2013. 184 p. [in Ukrainian] | ||||
| 3. Dunham K, Siriphorn A, Chompoopong S, et al. Characterization of a graded cervical hemicontusion spinal cord injury model in adult male rats. J Neurotrauma. 2010; 27(11): 2091-106. https://doi.org/10.1089/neu.2010.1424 PMid:21087156 PMCid:PMC2978055 | ||||
| 4. Griffiths IR. Vasogenic edema following acute and chronic spinal cord compression in the dog. J Neurosurg. 1975; 42(2): 155-165. https://doi.org/10.3171/jns.1975.42.2.0155 PMid:1113150 | ||||
| 5. Koyanagi I, Tator CH, Theriault E. Silicone rubber microangiography of acute spinal cord injury in the rat. Neurosurgery. 1993; 32(2): 260-68. https://doi.org/10.1097/00006123-199302000-00015 https://doi.org/10.1227/00006123-199302000-00015 PMid:8437664 | ||||
| 6. Tatagiba M, Brösamle C, Schwab ME. Regeneration of injured axons in the adult mammalian central nervous system. Neurosurgery. 1997; 40(3): 546-47. https://doi.org/10.1097/00006123-199703000-00023 https://doi.org/10.1227/00006123-199703000-00023 | ||||
| 8. Brodkey JS, Richards DE, Blasingame JP, et al. Reversible spinal cord trauma in cats. Additive effects of direct pressure and ischemia. J Neurosurg. 1972; 37(5): 591-93. https://doi.org/10.3171/jns.1972.37.5.0591 PMid:5076377 | ||||
| 9. Chen A, Xu XM, Kleitman N, et al. Methylprednisolone administration improves axonal regeneration into Schwann cell grafts in transected adult rat thoracic spinal cord. Exp Neurol. 1996; 138(2): 261-76. https://doi.org/10.1006/exnr.1996.0065 PMid:8620925 | ||||
| 10. Fawcett JW. Spinal cord repair: from experimental models to human application. Spinal Cord. 1998; 36(12): 811-17. https://doi.org/10.1038/sj.sc.3100769 PMid:9881728 | ||||
| 11. Tsymbaliuk VI, Medvediev VV. Spinnoy mozg. Elegiya nadezhdy: monografiya [Spinal cord. Elegy of hope: a monograph]. Vinnitsa: Nova Kniga – Vinnitsa: New Book, 2010. 944 p. [in Russian] | ||||
| 12. Hulsebosch CE. Recent advances in pathophysiology and treatment of spinal cord injury. Adv Physiol Educ. 2002; 26(1-4): 238-55. https://doi.org/10.1152/advan.00039.2002 PMid:12443996 | ||||
| 13. Carmel JB, Galante A, Soteropoulos P, et al. Gene expression profiling of acute spinal cord injury reveals spreading inflammatory signals and neuron loss. Physiol Genomics. 2001; 7(2): 201-13. https://doi.org/10.1152/physiolgenomics.00074.2001 PMid:11773606 | ||||
| 14. Bloom O. Non-mammalian model systems for studying neuro-immune interactions after spinal cord injury. Exp Neurol. 2014; 0: 113-30. https://doi.org/10.1016/j.expneurol.2013.12.023 | ||||
| 15. Ankarcrona M, Dypbukt J, Bonfoco E, et al.Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 1995; 15: 961-73. https://doi.org/10.1016/0896-6273(95)90186-8 | ||||
| 16. Sairanen T, Karjalainen-Lindsberg ML, Paetau A, et al. Apoptosis dominant in the periinfarct area of human ischemic stroke – a possible target of antiapoptotic treatments. Brain. 2006; 129(1): 189-99. https://doi.org/10.1093/brain/awh645 PMid:16272167 | ||||
| 17. Yuan J. Neuroprotective strategies targeting apoptotic and necrotic cell death for stroke. Apoptosis. 2009; 14(4): 469-77. https://doi.org/10.1007/s10495-008-0304-8 PMid:19137430 PMCid:PMC2745337 | ||||
| 18. Wang X, Li Y, Gao Y, et al. Combined use of spinal cord-mimicking partition type scaffold architecture and neurotrophin-3 for surgical repair of completely transected spinal cord in rats. J Biomater Sci Polym Ed. 2013; 24(8): 927-39. https://doi.org/10.1080/09205063.2012.727267 PMid:23647249 | ||||
| 19. Zeng X, Ma Y, Chen Y, et al. Autocrine fibronectin from differentiating mesenchymal stem cells induces the neurite elongation in vitro and promotes nerve fiber regeneration in transected spinal cord injury. J Biomed Mater Res A. 2016; 104(8): 1902-911. https://doi.org/10.1002/jbm.a.35720 PMid:26991461 PMCid:PMC5101622 | ||||
| 20. Khankan R, Griffis K, Haggerty-Skeans J, et al. Olfactory Ensheathing Cell Transplantation after a Complete Spinal Cord Transection Mediates Neuroprotective and Immunomodulatory Mechanisms to Facilitate Regeneration. J Neurosci. 2016; 36(23): 6269-286. https://doi.org/10.1523/JNEUROSCI.0085-16.2016 PMid:27277804 PMCid:PMC4899528 | ||||
| 21. Takiguchi M, Atobe Y, Kadota T, et al. Compensatory projections of primary sensory fibers in lumbar spinal cord after neonatal thoracic spinal transection in rats. Neuroscience. 2015; 304: 349-54. https://doi.org/10.1016/j.neuroscience.2015.07.046 PMid:26208841 | ||||
| 22. DePaul M, Lin C, Silver J, et al. Peripheral Nerve Transplantation Combined with Acidic Fibroblast Growth Factor and Chondroitinase Induces Regeneration and Improves Urinary Function in Complete Spinal Cord Transected Adult Mice. PLoS One. 2015; 10(10): 1-16. https://doi.org/10.1371/journal.pone.0139335 PMid:26426529 PMCid:PMC4591338 | ||||
| 23. Wada N, Shimizu T, Takai S, et al. Post-injury bladder management strategy in fl uences lower urinary tract dysfunction in the mouse model of spinal cord injury. Neurourol Urodynam. 2016. Available: http://www.sciencedirect.com/science/article/pii/S0361923016304944 | ||||
| 24. Oda Y, Tani K, Asari Y, et al. Canine Bone Marrow Stromal Cells Promote Functional Recovery in Mice with Spinal Cord Injury. J Vet Med Sci. 2014; 76(6): 905-908. https://doi.org/10.1292/jvms.13-0587 PMid:24561315 PMCid:PMC4108777 | ||||
| 25. Han S, Wang B, Li X, et al. Bone marrow-derived mesenchymal stem cells in three-dimensional culture promote neuronal regeneration by neurotrophic protection and immunomodulation. J Biomed Mater Res A. 2016; 104(7): 1759-769. https://doi.org/10.1002/jbm.a.35708 PMid:26990583 | ||||
| 26. Rao J, Yang Y, Lin S, et al. Repair of spinal cord injury by chitosan scaffold with glioma ECM and SB216763 implantation in adult rats. J Biomed Mater Res A. 2015; 103(10): 3259-272. https://doi.org/10.1002/jbm.a.35466 PMid:25809817 | ||||
| 27. Kanno H, Ozawa H, Tateda S, et al. Upregulation of the receptor-interacting protein 3 expression and involvement in neural tissue damage after spinal cord injury in mice. BMC Neurosci. 2015; 16(62): 1-10. https://doi.org/10.1186/s12868-015-0204-0 | ||||
| 28. Do-Thi A, Perrin F, Desclaux M, et al. Combination of grafted Schwann cells and lentiviral-mediated prevention of glial scar formation improve recovery of spinal cord injured rats. J Chem Neuroanat. 2016; 76: 48-60. https://doi.org/10.1016/j.jchemneu.2015.12.014 PMid:26744118 | ||||
| 29. Xiao W, Yu A, Liu D, et al. Ligustilide treatment promotes functional recovery in a rat model of spinal cord injury via preventing ROS production. Int J Clin Exp Pathol. 2015; 8(10): 12005-12013. PMid:26722386 PMCid:PMC4680331 | ||||
| 30. Tsymbaliuk V, Medvediev V, Rybachuk O, et al. The Effect of Implantation of Neurogeltm Used with Xenogenic Bone Marrow Stem Cells on Motor Function Recovery after Experimental Spinal Cord Injury. Int Neurol J. 2016; 84(6): 13-19. https://doi.org/10.22141/2224-0713.6.84.2016.83117 | ||||
| 31. Tsymbaliuk V, Medvediev V, Semenova V, et al. Clinical and pathomorphological features of penetrating spinal cord injury model with prolonged persistence of a foreign body in the vertebral canal. Ukr Neurosurg J. 2016; 4: 16-25. https://doi.org/10.25305/unj.86577 | ||||
| 32. Tsymbaliuk V, Medvediev V, Semenova V, et al. The model of lateral spinal cord hemisection. Part I. The technical, pathomorphological, clinical and experimental peculiarities. Ukr Neurosurg J. 2016; 7: 18-27. https://doi.org/10.25305/unj.72605 | ||||
| 33. Albadawi H, Chen J, Oklu R, et al. Spinal Cord Inflammation: Molecular Imaging after Thoracic Aortic Ischemia Reperfusion Injury. Radiology. 2017; 282(1): 202-211. https://doi.org/10.1148/radiol.2016152222 PMid:27509542 | ||||
| 34. Nguyen B, Albadawi H, Oklu R, et al. Ethyl pyruvate modulates delayed paralysis following thoracic aortic ischemia reperfusion in mice. J Vasc Surg. 2016; 64(5): 1433-443. https://doi.org/10.1016/j.jvs.2015.06.214 PMid:27776698 | ||||
| 35. Bell M, Puskas F, Bennett D, et al. Clinical indicators of paraplegia underplay universal spinal cord neuronal injury from transient aortic occlusion. Brain Res. 2015. Available: http://www.sciencedirect.com/science/article/pii/S0006899315003674 | ||||
| 36. Li H, Choudhury G, Zhang N, et al. Photothrombosis-induced focal ischemia as a model of spinal cord injury in mice. J Vis Exp. 2015. Available: http://www.jove.com/video/53161/photothrombosis-induced-focal-ischemia-as-model-spinal-cord-injury | ||||
| 37. Batista C, Bianqui L, Zanon B, et al. Behavioral improvement and regulation of molecules related to neuroplasticity in ischemic rat spinal cord treated with PEDF. Neural Plast. 2014. Available: https://www.hindawi.com/journals/np/2014/451639/ | ||||
| 38. Piao M, Lee J, Jang J, et al. Melatonin improves functional outcome via inhibition of matrix metalloproteinases-9 after photothrombotic spinal cord injury in rats. Acta Neurochir. (Wien). 2014; 156(11): 2173-182. https://doi.org/10.1007/s00701-014-2119-4 PMid:24879621 | ||||
| 39. Farahabadi A, Akbari M, Pishva A, et al. Effect of Progesterone Therapy on TNF-α and iNOS Gene Expression in Spinal Cord Injury Model. Acta Med Iran. 2016; 54(6): 345-51. PMid:27306339 | ||||
| 40. Fan H, Chen K, Duan L, et al. Beneficial effects of early hemostasis on spinal cord injury in the rat. Spinal Cord. 2016; 54(11): 924-32. https://doi.org/10.1038/sc.2016.58 https://doi.org/10.1038/sc.2016.97 | ||||
| 41. Aydin H, Ozkara E, Ozbek Z, et al. Histopathological evaluation of the effects of CAPE in experimental spinal cord injury. Turk Neurosurg. 2016; 26(3): 437-44. PMid:27161473 | ||||
| 42. Wu J, Maoqiang L, Fan H, et al. Rutin attenuates neuroinflammation in spinal cord injury rats. J Surg Res. 2016; 203(2): 331-37. https://doi.org/10.1016/j.jss.2016.02.041 PMid:27363641 | ||||
| 43. Farsi L, Afshari K, Keshavarz M, et al. Postinjury treatment with magnesium sulfate attenuates neuropathic pains following spinal cord injury in male rats. Behav Pharmacol. 2015; 26(3): 315-20. https://doi.org/10.1097/FBP.0000000000000103 PMid:25369748 | ||||
| 44. Ruzicka J, Machova-Urdzikova L, Gillick J, et al. A comparative study of three different types of stem cells for treatment of rat spinal cord injury. Cell Transplant. 2016; 1(914): 1-51. | ||||
| 45. Vanický I, Urdzíková L, Saganová K, et al. A simple and reproducible model of spinal cord injury induced by epidural balloon inflation in the rat. J Neurotrauma. 2001; 18(12): 1399-407. https://doi.org/10.1089/08977150152725687 PMid:11780869 | ||||
| 46. Morris S, Howard J, Rasmusson D, et al. Validity of Transcranial Motor Evoked Potentials as Early Indicators of Neural Compromise in Rat Model of Spinal Cord Compression. Spine. 2015; 40(8): 492-497. https://doi.org/10.1097/BRS.0000000000000808 PMid:25868103 | ||||
| 47. Rosene F, Raul M, Bressan B, et al. Transplantation of Human Skin-Derived Mesenchymal Stromal Cells Improves Locomotor Recovery After Spinal Cord Injury in Rats. Cell Mol Neurobiol. 2016. Available: https://link.springer.com/article/10.1007%2Fs10571-016-0414-8 | ||||
| 48. Allen AR. Surgery of experimental lesion of spinal cord an equivalent to crush injury of fracture dislocation of spinal column Preliminary Report. JAMA. 1911; 57: 878-80. https://doi.org/10.1001/jama.1911.04260090100008 | ||||
| 49. Keller AV, Wainwright G, Shum-Siu A, et al. Disruption of locomotion in response to hindlimb muscle stretch at acute and chronic time points after a spinal cord injury in rats. J Neurotrauma. 2017; 34(3): 661-70. https://doi.org/10.1089/neu.2015.4227 PMid:27196003 | ||||
| 50. Caudle KL, Atkinson DA, Brown EH, et al. Hindlimb Stretching Alters Locomotor Function After Spinal Cord Injury in the Adult Rat. Neurorehabil Neural Repair. 2015; 29(3): 268-77. https://doi.org/10.1177/1545968314543500 PMid:25106555 PMCid:PMC4312740 | ||||
| 51. Zhang S, Huang F, Gates M, et al. Early application of tail nerve electrical stimulation-induced walking training promotes locomotor recovery in rats with spinal cord injury. Spinal Cord. 2016; 54(11): 942-46. https://doi.org/10.1038/sc.2016.30 PMid:27067652 PMCid:PMC5399155 | ||||
| 52. Magnuson DS, Trinder TC, Zhang YP, et al. Comparing deficits following excitotoxic and contusion injuries in the thoracic and lumbar spinal cord of the adult rat. Exp Neurol. 1999; 156(1): 191-204. https://doi.org/10.1006/exnr.1999.7016 PMid:10192790 | ||||
| 53. Carelli S, Giallongo T, Gerace C, et al. Neural Stem Cell Transplantation in Experimental Contusive Model of Spinal Cord Injury. J Vis Exp. 2014. Available: http://www.jove.com/video/52141/neural-stem-cell-transplantation-experimental-contusive-model-spinal | ||||
| 54. Knerlich-Lukoschus F, Krossa S, Krause J, et al. Impact of chemokines on the properties of spinal cord-derived neural progenitor cells in a rat spinal cord lesion model. J Neurosci Res. 2015; 93(4): 562-71. https://doi.org/10.1002/jnr.23527 PMid:25491360 | ||||
| 55. Knerlich-Lukoschus F, Juraschek M, Blömer U, et al. Force-dependent development of neuropathic central pain and time-related CCL2/CCR2 expression after graded spinal cord contusion injuries of the rat. J Neurotrauma. 2008; 25(5): 427-48. https://doi.org/10.1089/neu.2007.0431 PMid:18338959 | ||||
| 56. Murakami T, Kanchiku T, Suzuki H, et al. Anti-interleukin-6 receptor antibody reduces neuropathic pain following spinal cord injury in mice. Exp Ther Med. 2013; 6(5): 1194-198. https://doi.org/10.3892/etm.2013.1296 | ||||
| 57. Ohri SS, Maddie MA, Zhang Y, et al. Deletion of the pro-apoptotic endoplasmic reticulum stress response effector CHOP does not result in improved locomotor function after severe contusive spinal cord injury. J Neurotrauma. 2012; 29(3): 579-88. https://doi.org/10.1089/neu.2011.1940 PMid:21933012 PMCid:PMC3282015 | ||||
| 58. Zhang YP, Burke DA, Shields LB, et al. Spinal Cord Contusion Based on Precise Vertebral Stabilization and Tissue Displacement Measured by Combined Assessment to Discriminate Small Functional Differences. J Neurotrauma. 2008; 25(10): 1227-240. https://doi.org/10.1089/neu.2007.0388 PMid:18986224 PMCid:PMC2756607 | ||||
| 59. McEwen ML, Springer JE. Quantification of locomotor recovery following spinal cord contusion in adult rats. J Neurotrauma. 2006; 23(11): 1632-653. https://doi.org/10.1089/neu.2006.23.1632 PMid:17115910 | ||||
| 60. Brambilla R, Bracchi-Ricard V, Hu W., et al. Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J Exp Med. 2005; 202(1): 145-56. https://doi.org/10.1084/jem.20041918 PMid:15998793 PMCid:PMC2212896 | ||||
| 61. Chen J, Xu XM, Xu Z, et al. Animal models of acute neurological injuries. Humana Press, 2009: 425-439. https://doi.org/10.1007/978-1-60327-185-1 | ||||
| 62. Sroga JM, Jones TB, Kigerl KA, et al. Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol. 2003; 462(2): 223-40. https://doi.org/10.1002/cne.10736 PMid:12794745 | ||||
| 63. Norenberg MD, Smith J, Marcillo A. The pathology of human spinal cord injury: defining the problems. J Neurotrauma. 2004; 21(4): 429-40. https://doi.org/10.1089/089771504323004575 PMid:15115592 | ||||
| 64. Stoppini L, Buchs PA, Muller D. A simple method for organotypic cultures of nervous tissue. Jornal of Neuroscience Methods. 1991; 37(2): 173-82. https://doi.org/10.1016/0165-0270(91)90128-M | ||||
| 65. Abu-Rub M, McMahon S, Zeugolis D, et al. Spinal cord injury in vitro: Modelling axon growth inhibition. Drug Discov Today. 2010; 15(11-12): 436-443. https://doi.org/10.1016/j.drudis.2010.03.008 PMid:20346411 | ||||
| 66. Lee M, Lee ES, Kim YS, et al. Ischemic Injury-Specific Gene Expression in the Rat Spinal Cord Injury Model Using Hypoxia-Inducible System. Spine. 2005; 30(24): 2729-734. https://doi.org/10.1097/01.brs.0000190395.43772.f3 PMid:16371895 | ||||
| 67. Shi R, Whitebone J. Conduction Deficits and Membrane Disruption of Spinal Cord Axons as a Function of Magnitude and Rate of Strain. J Neurophysiol. 2006; 95(6): 3384-390. https://doi.org/10.1152/jn.00350.2005 PMid:16510778 | ||||
| 68. Shearer MC, Niclou SP, Brown D, et al. The astrocyte/meningeal cell interface is a barrier to neurite outgrowth which can be overcome by manipulation of inhibitory molecules or axonal signaling pathways. Mol Cell Neurosci. 2003; 24(4): 913-25. https://doi.org/10.1016/j.mcn.2003.09.004 PMid:14697658 | ||||
| 69. Bregman BS, Mcatee M, Dai HN, et al. Neurotrophic Factors Increase Axonal Growth after Spinal Cord Injury and Transplantation in the Adult Rat. Experimental Neurology. 1997; 148(2): 475-94. https://doi.org/10.1006/exnr.1997.6705 PMid:9417827 | ||||
| 70. Taccola G, Mladinic M, Nistri A. Dynamics of early locomotor network dysfunction following a focal lesion in an in vitro model of spinal injury Eur J Neurosci. 2010; 31(1): 60-78. https://doi.org/10.1111/j.1460-9568.2009.07040.x PMid:20092556 | ||||
| 71. Mandadi S, Nakanishi S, Takashima Y, et al. Locomotor Networks are Targets of Modulation by Sensory Transient Receptor Potential Vanilloid 1 and Transient Receptor Potential Melastatin 8 Channels. Neuroscience. 2009; 162(4): 1377-397. https://doi.org/10.1016/j.neuroscience.2009.05.063 PMid:19482068 PMCid:PMC2880570 | ||||
| 72. Wanner IB, Deik A, Torres M, et al. A new in vitro model of the glial scar inhibits axon growth. Glia. 2008; 56(15): 1691-709. https://doi.org/10.1002/glia.20721 PMid:18618667 PMCid:PMC3161731 | ||||
| 73. Yoo JY, Hwang C, Hong HN. A Model of Glial Scarring Analogous to the Environment of a Traumatically Injured Spinal Cord Using Kainate. Department of Rehabilitation Medicine. 2016; 40(5): 757-68. https://doi.org/10.5535/arm.2016.40.5.757 PMid:27847705 PMCid:PMC5108702 | ||||
| 74. East E, Golding J, Phillips J. A versatile 3D culture model facilitates monitoring of astrocytes undergoing reactive gliosis. J Tissue Eng Regen Med. 2009; 3(8): 634-46. https://doi.org/10.1002/term.209 PMid:19813215 PMCid:PMC2842570 | ||||
| 75. Vyas A, Li Z, Aspalter M, et al. An in vitro model of adult mammalian nerve repair. Exp Neurol. 2010; 223(1): 112-18. https://doi.org/10.1016/j.expneurol.2009.05.022 PMid:19464291 PMCid:PMC2849894 | ||||
| 76. Buss A, Pech K, Kakulas BA, et al. TGF-β1 and TGF-β2 expression after traumatic human spinal cord injury. J Spinal Cord. 2007; 46(5): 364-71. https://doi.org/10.1038/sj.sc.3102148 PMid:18040277 | ||||
Rybachuk OA, Arkhypchuk IV, Lazarenko YuA. In vivo and in vitro models of traumatic injuries of the spinal cord. Cell and Organ Transplantology. 2017; 5(1):87-93. doi:10.22494/cot.v5i1.71
