Comparative model of minimal spinal cord injury reveals a rather anti-inflammatory response in the lesion site as well as increased proliferation in the central canal lining in the neonates compared to the adult rats.

التفاصيل البيبلوغرافية
العنوان:	Comparative model of minimal spinal cord injury reveals a rather anti-inflammatory response in the lesion site as well as increased proliferation in the central canal lining in the neonates compared to the adult rats.
المؤلفون:	Ševc J; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic., Mochnacký F; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic., Košuth J; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic., Alexovič Matiašová A; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic., Slovinská L; Faculty of Medicine, Associated Tissue Bank, P. J. Šafárik University in Košice and L. Pasteur University Hospital, Košice, Slovak Republic.; Institute of Neurobiology, Biomedical Research Center, Slovak Academy of Sciences, Košice, Slovak Republic., Blaško J; Institute of Neurobiology, Biomedical Research Center, Slovak Academy of Sciences, Košice, Slovak Republic., Bukhun I; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic., Holota R; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic., Tomori Z; Institute of Experimental Physics, Slovak Academy of Sciences, Košice, Slovak Republic., Daxnerová Z; Faculty of Science, Institute of Biology and Ecology, P. J. Šafárik University in Košice, Košice, Slovak Republic.
المصدر:	Developmental neurobiology [Dev Neurobiol] 2024 Jul; Vol. 84 (3), pp. 169-190. Date of Electronic Publication: 2024 May 29.
نوع المنشور:	Journal Article; Comparative Study
اللغة:	English
بيانات الدورية:	Publisher: Wiley Subscription Services, Inc Country of Publication: United States NLM ID: 101300215 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1932-846X (Electronic) Linking ISSN: 19328451 NLM ISO Abbreviation: Dev Neurobiol Subsets: MEDLINE
أسماء مطبوعة:	Original Publication: Hoboken, NJ : Wiley Subscription Services, Inc.
مواضيع طبية MeSH:	Spinal Cord Injuries/immunology , Spinal Cord Injuries/pathology , Spinal Cord Injuries/physiopathology , Rats, Wistar , Disease Models, Animal* , Animals, Newborn* , Cell Proliferation*/physiology, Animals ; Rats ; Spinal Cord/pathology ; Spinal Cord/immunology ; Astrocytes/pathology ; Female
مستخلص:	Spinal cord injury (SCI) resulting from trauma decreases the quality of human life. Numerous clues indicate that the limited endogenous regenerative potential is a result of the interplay between the inhibitory nature of mature nervous tissue and the inflammatory actions of immune and glial cells. Knowledge gained from comparing regeneration in adult and juvenile animals could draw attention to factors that should be removed or added for effective therapy in adults. Therefore, we generated a minimal SCI (mSCI) model with a comparable impact on the spinal cord of Wistar rats during adulthood, preadolescence, and the neonatal period. The mechanism of injury is based on unilateral incision with a 20 ga needle tip according to stereotaxic coordinates into the dorsal horn of the L4 lumbar spinal segment. The incision should harm a similar amount of gray matter on a coronal section in each group of experimental animals. According to our results, the impact causes mild injury with minimal adverse effects on the neurological functions of animals but still has a remarkable effect on nervous tissue and its cellular and humoral components. Testing the mSCI model in adults, preadolescents, and neonates revealed a rather anti-inflammatory response of immune cells and astrocytes at the lesion site, as well as increased proliferation in the central canal lining in neonates compared with adult animals. Our results indicate that developing nervous tissue could possess superior reparative potential and confirm the importance of comparative studies to advance in the field of neuroregeneration. (© 2024 Wiley Periodicals LLC.)
References:	Alexovič Matiašová, A., Ševc, J., Tomori, Z., Gombalová, Z., Gedrová, Š., & Daxnerová, Z. (2017). Quantitative analyses of cellularity and proliferative activity reveals the dynamics of the central canal lining during postnatal development of the rat. Journal of Comparative Neurology, 525(3), 693–707. https://doi.org/10.1002/cne.24091. Barnabé‐Heider, F., Goritz, C., Sabelstrom, H., Takebayashi, H., Pfrieger, F. W., Meletis, K., & Frisen, J. (2010). Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell, 7(4), 470–482. https://doi.org/10.1016/j.stem.2010.07.014. Basso, D. M., Beattie, M. S., & Bresnahan, J. C. (1995). A sensitive and reliable locomotor rating scale for open field testing in rats. Journal of Neurotrauma, 12(1), 1–21. https://doi.org/10.1089/neu.1995.12.1. Blaško, J., Szekiová, E., Slovinská, L., Kafka, J., & Čížková, D. (2017). Axonal outgrowth stimulation after alginate/mesenchymal stem cell therapy in injured rat spinal cord. Acta Neurobiologiae Experimentalis, 77(4), 337–350. https://doi.org/10.21307/ane‐2017‐066. Bravo‐Hernandez, M., Tadokoro, T., Navarro, M. R., Platoshyn, O., Kobayashi, Y., Marsala, S., Miyanohara, A., Juhas, S., Juhasova, J., Skalnikova, H., Tomori, Z., Vanicky, I., Studenovska, H., Proks, V., Chen, P., Govea‐Perez, N., Ditsworth, D., Ciacci, J. D., Gao, S., … Marsala, M. (2020). Spinal subpial delivery of AAV9 enables widespread gene silencing and blocks motoneuron degeneration in ALS. Nature Medicine, 26(1), 118–130. https://doi.org/10.1038/s41591‐019‐0674‐1. Bregman, B. S., & Goldberger, M. E. (1983). Infant lesions effect: I. Development of motor behavior following neonatal spinal cord damage in cats. Developmental Brain Research, 9, 103–117. https://doi.org/10.1016/0165‐3806(83)90045‐7. Chevreau, R., Ghazale, H., Ripoll, C., Chalfouh, C., Delarue, Q., Hemonnot‐Girard, A. L., Hirbec, H., Wahane, S., Perrin, F., Noristani, H., Guerout, N., & Hugnot, J. P. (2021). Reaction of ependymal cells to spinal cord injury: A potential role for oncostatin pathway and microglial cells. BioRxiv, 2021–2032. https://doi.org/10.1101/2021.02.12.428106. Cigliola, V., Shoffner, A., Lee, N., Ou, J., Gonzalez, T. J., Hoque, J., Becker, C. J., Han, Y., Shen, G., Faw, T. D., Abd‐El‐Barr, M. M., Varghese, S., Asokan, A., & Poss, K. D. (2023). Spinal cord repair is modulated by the neurogenic factor Hb‐egf under direction of a regeneration‐associated enhancer. Nature Communications, 14(1), 4857. https://doi.org/10.1038/s41467‐023‐40486‐5. Coskun, V., Wu, H., Blanchi, B., Tsao, S., Kim, K., Zhao, J., Biancotti, J. C., Hutnick, L., Krueger, R. C., Fan, G., de Vellis, J., & Sun, Y. E. (2008). CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proceedings of the National Academy of Sciences of the United States of America, 105, 1026–1031. https://doi.org/10.1073/pnas.0710000105. Galvan, M. D., Luchetti, S., Burgos, A. M., Nguyen, H. X., Hooshmand, M. J., Hamers, F. P. T., & Anderson, A. J. (2008). Deficiency in complement C1q improves histological and functional locomotor outcome after spinal cord injury. Journal of Neuroscience, 28(51), 13876–13888. https://doi.org/10.1523/JNEUROSCI.2823‐08.2008. Ghazale, H., Ripoll, C., Leventoux, N., Jacob, L., Azar, S., Mamaeva, D., Glasson, Y., Calvo, C. F., Thomas, J. L., Meneceur, S., Lallemand, Y., Rigau, V., Perrin, F. E., Noristani, H. N., Rocamonde, B., Huillard, E., Bauchet, L., & Hugnot, J. P. (2019). RNA profiling of the human and mouse spinal cord stem cell niches reveals an embryonic‐like regionalization with MSX1(+) roof‐plate‐derived cells. Stem Cell Reports, 12, 1159–1177. https://doi.org/10.1016/j.stemcr.2019.04.001. Grulová, I., Slovinská, L., Blaško, J., Devaux, S., Wisztorski, M., Salzet, M., Fournier, I., Kryukov, O., Cohen, S., & Čížková, D. (2015). Delivery of alginate scaffold releasing two trophic factors for spinal cord injury repair. Scientific Reports, 5, 13702. https://doi.org/10.1038/srep13702. Hachem, L. D., Mothe, A. J., & Tator, C. H. (2020). Unlocking the paradoxical endogenous stem cell response after spinal cord injury. Stem Cells, 38(2), 187–194. https://doi.org/10.1002/stem.3107. Hamers, F. P., Lankhorst, A. J., van Laar, T. J., Veldhuis, W. B., & Gispen, W. H. (2001). Automated quantitative gait analysis during overground locomotion in the rat: Its application to spinal cord contusion and transection injuries. Journal of Neurotrauma, 18(2), 187–201. https://doi.org/10.1089/08977150150502613. Hasegawa, A., Takahashi, M., Satomi, K., Ohne, H., Takeuchi, T., Sato, S., & Ichimura, S. (2016). Mechanism of forelimb motor function restoration after cervical spinal cord hemisection in rats: A comparison of juveniles and adults. Behavioral Neurology, 1035473. https://doi.org/10.1155/2016/1035473. Huang, W., Bai, X., Stopper, L., Catalin, B., Cartarozzi, L. P., Scheller, A., & Kirchhoff, F. (2018). During development NG2 glial cells of the spinal cord are restricted to the oligodendrocyte lineage, but generate astrocytes upon acute injury. Neuroscience, 385, 154–165. https://doi.org/10.1016/j.neuroscience.2018.06.015. Johansson, C. B., Momma, S., Clarke, D. L., Risling, M., Lendahl, U., & Frisen, J. (1999). Identification of a neural stem cell in the adult mammalian central nervous system. Cell, 96(1), 25–34. https://doi.org/10.1016/s0092‐8674(00)80956‐3. King, N. M., & Perrin, J. (2014). Ethical issues in stem cell research and therapy. Stem Cell Research & Therapy, 5, 85. https://doi.org/10.1186/scrt474. Kitade, K., Kobayakawa, K., Saiwai, H., Matsumoto, Y., Kawaguchi, K., Iida, K., Kijima, K., Iura, H., Tamaru, T., Haruta, Y., Ono, G., Konno, D., Maeda, T., Okada, S., Nakashima, K., & Nakashima, Y. (2023). Reduced neuroinflammation via astrocytes and neutrophils promotes regeneration after spinal cord injury in neonatal mice. Journal of Neurotrauma, 40(23–24), 2566–2579. https://doi.org/10.1089/neu.2023.0044. Košuth, J., Farkašovská, M., Mochnacký, F., Daxnerová, Z., & Ševc, J. (2020). Selection of reliable reference genes for analysis of gene expression in spinal cord during rat postnatal development and after injury. Brain Sciences, 10, 6. https://doi.org/10.3390/brainsci10010006. Lau, N. S. S., Gorrie, C. A., Chia, J. Y., Bilston, L. E., & Clarke, E. C. (2013). Severity of spinal cord injury in adult and infant rats after vertebral dislocation depends upon displacement but not speed. Journal of Neurotrauma, 30(15), 1361–1373. https://doi.org/10.1089/neu.2012.2725. Li, X., Floriddia, E. M., Toskas, K., Fernandes, K. J. L., Guerout, N., & Barnabé‐Heider, F. (2016). Regenerative potential of ependymal cells for spinal cord injuries over time. EBioMedicine, 13, 55–65. https://doi.org/10.1016/j.ebiom.2016.10.035. Li, Y., He, X., Kawaguchi, R., Zhang, Y., Wang, Q., Monavarfeshani, A., Yang, Z., Chen, B., Shi, Z., Meng, H., Zhou, S., Zhu, J., Jacobi, A., Swarup, V., Popovich, P. G., Geschwind, D. H., & He, Z. (2020). Microglia‐organized scar‐free spinal cord repair in neonatal mice. Nature, 587(7835), 613–618. https://doi.org/10.1038/s41586‐020‐2795‐6. Marsala, M., Kamizato, K., Tadokoro, T., Navarro, M. R., Juhás, Š., Juhásová, J., Marsala, S., Studenovska, H., Proks, V., Hazel, T., Johe, K., Kakinohana, M., Driscoll, S., Glenn, T., Pfaff, S., & Ciacci, J. (2020). Spinal parenchymal occupation by neural stem cells after subpial delivery in adult immunodeficient rats. Stem Cells Translational Medicine, 9(2), 177–188. https://doi.org/10.1002/sctm.19‐0156. McDonough, A., & Martinez‐Cerdeno, V. (2012). Endogenous proliferation after spinal cord injury in animal models. Stem Cells International, 2012, 387513. https://doi.org/10.1155/2012/387513. Meletis, K., Barnabé‐Heider, F., Carlén, M., Evergren, E., Tomilin, N., Shupliakov, O., & Frisén, J. (2008). Spinal Cord Injury Reveals Multilineage Differentiation of Ependymal Cells. PLoS Biology, 6(7), e182. https://doi.org/10.1371/journal.pbio.0060182. Ming, G., & Song, H. (2011). Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions. Neuron, 70(4), 687–702. https://doi.org/10.1016/j.neuron.2011.05.001. Minett, M. S., Eijkelkamp, N., & Wood, J. N. (2014). Significant determinants of mouse pain behaviour. PLoS ONE, 9(8), e104458. https://doi.org/10.1371/journal.pone.0104458. Moulson, A. J., Squair, J. W., Franklin, R. J. M., Tetzlaff, W., & Assinck, P. (2021). Diversity of Reactive Astrogliosis in CNS Pathology: Heterogeneity or Plasticity? Frontiers in Cellular Neuroscience, 15. https://doi.org/10.3389/fncel.2021.703810. Mothe, A. J., & Tator, C. H. (2005). Proliferation, migration, and differentiation of endogenous ependymal region stem/progenitor cells following minimal spinal cord injury in the adult rat. Neuroscience, 131(1), 177–187. https://doi.org/10.1016/j.neuroscience.2004.10.011. Musselman, K. E., Shah, M., & Zariffa, J. (2018). Rehabilitation technologies and interventions for individuals with spinal cord injury: Translational potential of current trends. Journal of NeuroEngineering and Rehabilitation, 15(1), 40. https://doi.org/10.1186/s12984‐018‐0386‐7. Okano, H., Okada, S., Nakamura, M., & Toyama, Y. (2005). Neural stem cells and regeneration of injured spinal cord. Kidney International, 68(5), 927–931. https://doi.org/10.1111/j.1523‐1755.2005.00621.x. O'Shea, T. M., Burda, J. E., & Sofroniew, M. V. (2017). Cell biology of spinal cord injury and repair. Journal of Clinical Investigation, 127(9), 3259–3270. https://doi.org/10.1172/JCI90608. Pape, K. E. (2012). Developmental and maladaptive plasticity in neonatal SCI. Clinical Neurology and Neurosurgery, 114, 475–482. https://doi.org/10.1016/j.clineuro.2012.01.002. Peretto, P., & Bonfanti, L. (2014). Major unsolved points in adult neurogenesis: Doors open on a translational future? Frontiers in Neuroscience, 8, 1–6. https://doi.org/10.3389/fnins.2014.00154. Ren, Y., Ao, Y., O'Shea, T. M., Burda, J. E., Bernstein, A. M., Brumm, A. J., Muthusamy, N., Ghashghaei, H. T., Carmichael, S. T., Cheng, L., & Sofroniew, M. V. (2017). Ependymal cell contribution to scar formation after spinal cord injury is minimal, local and dependent on direct ependymal injury. Scientific Reports, 7, 41122. https://doi.org/10.1038/srep41122. Rodríguez‐Barrera, R., Rivas‐González, M., García‐Sánchez, J., Mojica‐Torres, D., & Ibarra, A. (2021). Neurogenesis after spinal cord injury: State of the Art. Cells, 10, 1499. https://doi.org/10.3390/cells10061499. Sabelstrom, H., Stenudd, M., Reu, P., Dias, D. O., Elfineh, M., Zdunek, S., Damberg, P., Goritz, C., & Frisen, J. (2013). Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science, 342(6158), 637–640. https://doi.org/10.1126/science.1242576. Sabourin, J. C., Ackema, K. B., Ohayon, D., Guichet, P. O., Perrin, F. E., Garces, A., Ripoll, C., Charité, J., Simonneau, L., Kettenmann, H., Zine, A., Privat, A., Valmier, J., Pattyn, A., & Hugnot, J. P. (2009). A mesenchymal‐like ZEB1+ niche harbors dorsal radial glial fibrillary acidic protein‐positive stem cells in the spinal cord. Stem Cells, 27(11), 2722–2733. https://doi.org/10.1002/stem.226. Scholz, J., Broom, D. C., Youn, D. H., Kohno, T., Suter, M. R., Moore, K. A., Decosterd, I., Coggeshall, R. E., & Woolf, C. J. (2005). Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury. Journal of Neuroscience, 25(32), 7317–7323. https://doi.org/10.1523/JNEUROSCI.1526‐05.2005. Ševc, J., Daxnerová, Z., Haňová, V., & Koval', J. (2011). Novel observations on the origin of ependymal cells in the ventricular zone of the rat spinal cord. Acta Histochemica, 113(2), 156–162. https://doi.org/10.1016/j.acthis.2009.09.007. Ševc, J., Matiašová, A., Kútna, V., & Daxnerová, Z. (2014). Evidence that the central canal lining of the spinal cord contributes to oligodendrogenesis during postnatal development and adulthood in intact rats. Journal of Comparative Neurology, 522(14), 3194–3207. https://doi.org/10.1002/cne.23590. Shihabuddin, L. S., Horner, P. J., Ray, J., & Gage, F. H. (2000). Adult spinal cord stem cells generate neurons after transplantation in the adult dentate gyrus. Journal of Neuroscience, 20, 8727–8735. https://doi.org/10.1523/JNEUROSCI.20‐23‐08727.2000. Singh, A., Tetreault, L., Kalsi‐Ryan, S., Nouri, A., & Fehlings, M. G. (2014). Global prevalence and incidence of traumatic spinal cord injury. Clinical Epidemiology, 6, 309–331. https://doi.org/10.2147/CLEP.S68889. Slovinská, L., Szekiová, E., Blaško, J., Devaux, S., Salzet, M., & Čížková, D. (2015). Comparison of dynamic behavior and maturation of neural multipotent cells derived from different spinal cord developmental stages: An in vitro study. Acta Neurobiologiae Experimentalis, 75(1), 107–114. Sofroniew, M. V. (2020). Astrocyte reactivity: Subtypes, states, and functions in CNS innate immunity. Trends in Immunology, 41, 758–770. https://doi.org/10.1016/j.it.2020.07.004. Sutherland, T. C., Mathews, K. J., Mao, Y., Nguyen, T., & Gorrie, C. A. (2017). Differences in the cellular response to acute spinal cord injury between developing and mature rats highlights the potential significance of the inflammatory response. Frontiers in Cellular Neuroscience, 10, 310. https://doi.org/10.3389/fncel.2016.00310. Sutherland, T. C., Ricafrente, A., Gomola, K., O'Brien, B. A., & Gorrie, C. A. (2021). Neonatal rats exhibit a predominantly anti‐inflammatory response following spinal cord injury. Developmental Neuroscience, 43, 18–26. https://doi.org/10.1159/000514612. Tator, C. (2002). Strategies for recovery and regeneration after brain and spinal cord injury. Injury Prevention, 8(Suppl4), iv33–iv36. https://doi.org/10.1136/ip.8.suppl_4.iv33. Tran, A. P., Warren, P. M., & Silver, J. (2022). New insights into glial scar formation after spinal cord injury. Cell and Tissue Research, 378, 319–336. https://doi.org/10.1007/s00441‐021‐03477‐w. Walker, S. M., & Yaksh, T. (2012). Neuraxial analgesia in neonates and infants: A review of clinical and preclinical strategies for the development of safety and efficacy data. Anesthesia & Analgesia, 115(3), 638–662. https://doi.org/10.1213/ANE.0b013e31826253f2. Waller, R., Baxter, L., Fillingham, D. J., Coelho, S., Pozo, J. M., Mozumder, M., Frangi, A. F., Ince, P. G., Simpson, J. E., & Highley, J. R. (2019). Iba‐1‐/CD68+ microglia are a prominent feature of age‐associated deep subcortical white matter lesions. PLoS ONE, 14(1), e0210888. https://doi.org/10.1371/journal.pone.0210888. Watson, C., Paxinos, G., Kayalioglu, G., & Heise, C. (2009). Chapter 15 ‐ Atlas of the rat spinal cord. In The spinal cord (pp. 238–306). Academic Press. https://doi.org/10.1016/B978‐0‐12‐374247‐6.50019‐5. Wingrave, J. M., Sribnick, E. A., Wilford, G. G., Matzelle, D. D., Mou, J. A., Ray, S. K., Hogan, E. L., & Banik, N. L. (2004). Relatively low levels of calpain expression in juvenile rat correlate with less neuronal apoptosis after spinal cord injury. Experimental Neurology, 187(2), 529–532. https://doi.org/10.1016/j.expneurol.2004.02.001. Yuan, Q., Su, H., Chiu, K., Wu, W., & Lin, Z.‐X. (2013). Contrasting neuropathology and functional recovery after spinal cord injury in developing and adult rats. Neuroscience Bulletin, 29, 509–516. https://doi.org/10.1007/s12264‐013‐1356‐5.
معلومات مُعتمدة:	Vedecká Grantová Agentúra MŠVVaŠ SR a SAV; Agentúra na Podporu Výskumu a Vývoja
فهرسة مساهمة:	Keywords: development; glial scar; inflammation; neural stem cells; spinal cord injury
تواريخ الأحداث:	Date Created: 20240530 Date Completed: 20240716 Latest Revision: 20240716
رمز التحديث:	20240716
DOI:	10.1002/dneu.22942
PMID:	38812372
قاعدة البيانات:	MEDLINE

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تدمد:	1932-846X
DOI:	10.1002/dneu.22942