Neuroprotective response and efficacy of intravenous administration of mesenchymal stem cells in traumatic brain injury mice.

fluorescence in situ hybridisation magnetic resonance imaging mesenchymal stem cells neuronal differentiation traumatic brain injury

Journal

The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110

Informations de publication

Date de publication:
01 May 2021
Historique:
revised: 06 04 2021
received: 27 10 2019
accepted: 26 04 2021
pubmed: 2 5 2021
medline: 2 5 2021
entrez: 1 5 2021
Statut: aheadofprint

Résumé

Cellular transplantation of stem cells can be a beneficial treatment approach for neurodegenerative diseases such as traumatic brain injury (TBI). In this study, we investigated the proliferation and differentiation potential of infused mesenchymal stem cells (MSCs) after localisation at the injury site. We evaluated the appropriate homing of infused MSCs through immunohistochemistry, followed by Y-chromosome-specific polymerase chain reaction and fluorescent in situ hybridisation analyses. The proliferation and differentiation of infused MSCs were analysed using exogenous cell tracer 5'-bromo-2'-deoxyuridine (BrdU) labelling and neuronal specific markers, respectively. Structural and functional recovery in TBI mice were examined by performing magnetic resonance imaging and different behavioural assessments, respectively. Results demonstrated a significantly high number of BrdU-positive cells in the lesion region in the MSC-infused group compared with control and TBI groups. Infused MSCs were well differentiated into neural-like cells and expressed significantly more neural markers (neuronal nuclear antigen [NeuN], microtubule-associated protein 2 [MAP2] and glial fibrillary acid protein [GFAP]). Improved tissue abnormalities as well as functional behaviours were observed in MSC-infused TBI mice, implying the substantial proliferation and differentiation of infused MSCs. Our findings support the neuroprotective response and efficacy of MSCs after transplantation in TBI mice, and MSCs may serve as potential therapeutic candidates in regenerative medicine.

Identifiants

pubmed: 33932318
doi: 10.1111/ejn.15261
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2021 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Albert-Weissenberger, C., & Siren, A. L. (2010). Experimental traumatic brain injury. Exp Transl Stroke Med, 2, 16. https://doi.org/10.1186/2040-7378-2-16
Anbari, F., Khalili, M. A., Bahrami, A. R., Khoradmehr, A., Sadeghian, F., Fesahat, F., & Nabi, A. (2014). Intravenous transplantation of bone marrow mesenchymal stem cells promotes neural regeneration after traumatic brain injury. Neural Regen Res., 9, 919-923. https://doi.org/10.4103/1673-5374.133133
Baraniak, P.R., & McDevitt, T.C. (2010). Stem cell paracrine actions and tissue regeneration. Regenerative Medicine, 5(1), 121-143.
Bernardo, M. E., & Fibbe, W. E. (2013). Mesenchymal stromal cells: Sensors and switchers of inflammation. Cell Stem Cell, 13, 392-402. https://doi.org/10.1016/j.stem.2013.09.006
Blaiss, C. A., Yu, T.-S., Zhang, G., Chen, J., Dimchev, G., Parada, L. F., Powell, C. M., & Kernie, S. G. (2011). Temporally specified genetic ablation of neurogenesis impairs cognitive recovery after traumatic brain injury. Journal of Neuroscience, 31(13), 4906-4916. https://doi.org/10.1523/JNEUROSCI.5265-10.2011
Blennow, K., Hardy, J., & Zetterberg, H. (2012). The neuropathology and neurobiology of traumatic brain injury. Neuron, 76, 886-899. https://doi.org/10.1016/j.neuron.2012.11.021
Brooks, S. P., & Dunnett, S. B. (2009). Tests to assess motor phenotype in mice: A user’s guide. Nature Rev Neurosci, 10, 519-529.
Carlson, S. W., & Saatman, K. E. (2018). Central infusion of insulin-like growth factor-1 increases hippocampal neurogenesis and improves neurobehavioral function after traumatic brain injury. Journal of Neurotrauma, 35, 1467-1480. https://doi.org/10.1089/neu.2017.5374
Cox, C. S. Jr, Juranek, J., & Bedi, S. (2019). Clinical trials in traumatic brain injury: Cellular therapy and outcome measures. Transfusion, 59(S1), 858-868. https://doi.org/10.1111/trf.14834
Dantuma, E., Merchant, S., & Sugaya, K. (2010). Stem cells for the treatment of neurodegenerative diseases. Stem Cell Research & Therapy, 1, 37. https://doi.org/10.1186/scrt37
Deng, Y. B., Liu, X. G., Liu, Z. G., Liu, X. L., Liu, Y., & Zhou, G. Q. (2006). Implantation of BM mesenchymal stem cells into injured spinal cord elicits de novo neurogenesis and functional recovery: Evidence from a study in rhesus monkeys. Cytotherapy, 8, 210-214. https://doi.org/10.1080/14653240600760808
Dominici, M., Le Blanc, K., Mueller, I. Slaper-Cortenbach, I., Marini, F. C., Krause, D. S., Deans, R. J., Keating, A., Prockop, D. J. & Horwitz, E. M. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8(4), 315-317.
Galgano, M., Toshkezi, G., Qiu, X., Russell, T., Chin, L., & Zhao, L.-R. (2017). Traumatic brain injury: Current treatment strategies and future endeavors. Cell Transplantation, 26(7), 1118-1130. https://doi.org/10.1177/0963689717714102
Gutiérrez-Fernández, M., Rodríguez-Frutos, B., Álvarez-Grech, J., Vallejo-Cremades, M. T., Expósito-Alcaide, M., Merino, J., Roda, J. M., & Díez-Tejedor, E. (2011). Functional recovery after hematic administration of allogenic mesenchymal stem cells in acute ischemic stroke in rats. Neuroscience, 175, 394-405. https://doi.org/10.1016/j.neuroscience.2010.11.054
Hemphill, M. A., Dauth, S., Yu, C. J., Dabiri, B. E., & Parker, K. K. (2015). Traumatic brain injury and the neuronal microenvironment: A potential role for neuropathological mechanotransduction. Neuron, 85(6), 1177-1192. https://doi.org/10.1016/j.neuron.2015.02.041
Jackson, J. S., Golding, J. P., Chapon, C., Jones, W. A., & Bhakoo, K. K. (2010). Homing of stem cells to sites of inflammatory brain injury after intracerebral and intravenous administration: A longitudinal imaging study. Stem Cell Research & Therapy, 1, 17. https://doi.org/10.1186/scrt17
Karp, J. M., & Teo, G. S. L. (2009). Mesenchymal stem cell homing: The devil is in the detail. Cell Stem Cell, 4, 206-216.
Kinoshita, K. (2016). Traumatic brain injury: Pathophysiology for neurocritical care. Journal of Intensive Care, 4, 29. https://doi.org/10.1186/s40560-016-0138-3
Lim, J. Y., Jeong, C. H., Jun, J. A., Kim, S. M., Ryu, C. H., Hou, Y., Oh, W., Chang, J. W., & Jeun, S. S. (2011). Therapeutic effects of human umbilical cord blood-derived mesenchymal stem cells after intrathecal administration by lumbar puncture in a rat model of cerebral ischemia. Stem Cell Research & Therapy, 2, 38. https://doi.org/10.1186/scrt79
Lindvall, O., & Kokaia, Z. (2010). Stem cells in human neurodegenerative disorders-time for clinical translation? J Clin Invest., 120(1), 29-40. https://doi.org/10.1172/JCI40543
Lu, D., Mahmood, A., Changsheng, Q., Oussev, A., Schallert, T., Chopp, M. (2003). Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. Journal of Neurotrauma, 22, 1011-1017.
Lu, D., Mahmood, A., Qu, C., Goussev, A., Schallert, T., & Chopp, M. (2005). Erythropoietin enhances neurogenesis and restores spatial memory in rats after traumatic brain injury. Journal of Neurotrauma, 22(9), 1011-1017.
Ma, S., Xie, N., Li, W., Yuan, B., Shi, Y., & Wang, Y. (2014). Immunobiology of mesenchymal stem cells. Cell Death and Differentiation, 21, 216-225.
Maas, A. I. R., Menon, D. K., Adelson, P. D., Andelic, N., Bell, M. J., Belli, A., Bragge, P., Brazinova, A., Büki, A., Chesnut, R. M., Citerio, G., Coburn, M., Cooper, D. J., Crowder, A. T., Czeiter, E., Czosnyka, M., Diaz-Arrastia, R., Dreier, J. P., Duhaime, A.-C., … Zumbo, F. (2017). Traumatic brain injury: Integrated approaches to improve prevention, clinical care, and research. The Lancet Neurology, 16(12), 987-1048. https://doi.org/10.1016/S1474-4422(17)30371-X
Mahmood, A., Lu, D., & Chopp, M. (2004). Marrow stromal cell transplantation after traumatic brain injury promotes cellular proliferation within the brain. Neurosurgery, 55, 1185-1193.
Mishra, S. K., Khushu, S., & Gangenahalli, G. (2015). Potential stem cell labeling ability of poly-L-lysine complexed to ultrasmall iron oxide contrast agent: An optimization and relaxometry study. Experimental Cell Research, 339, 427-436.
Mishra, S. K., Khushu, S., & Gangenahalli, G. (2020). A distinctive MRI-based absolute bias correction protocol for the potential labelling and in vivo tracking of stem cells in a TBI mice model. Methods in Molecular Biology, 2150, 93-111. https://doi.org/10.1007/7651_2019_277
Mishra, S. K., Khushu, S., Singh, A. K., & Gangenahalli, G. (2018). Homing and tracking of iron oxide labelled mesenchymal stem cells after infusion in traumatic brain injury mice: A longitudinal in vivo MRI study. Stem Cell Review Report, 14, 888-900.
Mishra, S. K., Kumar, B. S. H., Khushu, S., Singh, A. K., & Gangenahalli, G. (2017). Early monitoring and quantitative evaluation of macrophage infiltration after experimental traumatic brain injury: A magnetic resonance imaging and flow cytometric analysis. Molecular and Cellular Neurosciences, 78, 25-34.
Mishra, S. K., Rana, P., Khushu, S., & Gangenahalli, G. (2017). Therapeutic prospective of infused allogenic cultured mesenchymal stem cells in traumatic brain injury mice: A longitudinal proton magnetic resonance spectroscopy assessment. Stem Cells Translational Medicine, 6, 316-329. https://doi.org/10.5966/sctm.2016-0087
Mohamadpour, M., Whitney, K., & Bergold, P. J. (2019). The importance of therapeutic time window in the treatment of traumatic brain injury. Frontiers in Neuroscience, 13, 07. https://doi.org/10.3389/fnins.2019.00007
Ngwenya, L. B., & Danzer, S. C. (2019). Impact of traumatic brain injury on neurogenesis. Frontiers in Neuroscience, 12, 1014. https://doi.org/10.3389/fnins.2018.01014
Park, K.J., Park, E., Liu, E., & Baker, A.J. (2014). Bone marrow derived endothelial progenitor cells protect postischemic axons after traumatic brain injury. Journal of Cerebral Blood Flow & Metabolism, 34(2), 357-366.
Prins, M., Greco, T., Alexander, D., & Giza, C. C. (2013). The pathophysiology of traumatic brain injury at a glance. Disease Models & Mechanisms, 6(6), 1307-1315. https://doi.org/10.1242/dmm.011585
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671-675.
Stein, D. G. (2015). Embracing failure: What the Phase III progesterone studies can teach about TBI clinical trials. Brain Injury, 29(11), 1259-1272. https://doi.org/10.3109/02699052.2015.1065344
Sun, D. (2014). The potential of endogenous neurogenesis for brain repair and regeneration following traumatic brain injury. Neural Regeneration Research, 9(7), 688-692. https://doi.org/10.4103/1673-5374.131567
Sun, D., Bullock, M. R., Altememi, N., Zhou, Z., Hagood, S., Rolfe, A., McGinn, M. J., Hamm, R., & Colello, R. J. (2010). The effect of epidermal growth factor in the injured brain after trauma in rats. Journal of Neurotrauma, 27, 923-938. https://doi.org/10.1089/neu.2009.1209
Sun, D., Bullock, M. R., McGinn, M. J., Zhou, Z., Altememi, N., Hagood, S., Hamm, R., & Colello, R. J. (2009). Basic fibroblast growth factor-enhanced neurogenesis contributes to cognitive recovery in rats following traumatic brain injury. Experimental Neurology, 216, 56-65. https://doi.org/10.1016/j.expneurol.2008.11.011
Sun, D., Daniels, T. E., Rolfe, A., Waters, M., & Hamm, R. (2015). Inhibition of injury-induced cell proliferation in the dentate gyrus of the hippocampus impairs spontaneous cognitive recovery after traumatic brain injury. Journal of Neurotrauma, 32(7), 495-505. https://doi.org/10.1089/neu.2014.3545
Willing, A. E., Das, M., Howell, M., Mohapatra, S. S., & Mohapatra, S. (2020). Potential of mesenchymal stem cells alone, or in combination, to treat traumatic brain injury. CNS Neuroscience & Therapeutics, 26(6), 616-627. https://doi.org/10.1111/cns.13300
Xiong, Y. E., Zhang, Y., Mahmood, A., & Chopp, M. (2015). Investigational agents for treatment of traumatic brain injury. Expert Opinion on Investigational Drugs, 24(6), 743-760. https://doi.org/10.1517/13543784.2015.1021919
Ye, Y., Peng, Y. R., Hu, S. Q., Yan, X. L., Chen, J., & Xu, T. (2016). In vitro differentiation of bone marrow mesenchymal stem cells into neuron-like cells by cerebrospinal fluid improves motor function of middle cerebral artery occlusion rats. Frontiers in Neurology, 7, 183.
Yoo, S. W., Kim, S. S., Lee, S. Y., Lee, H. S., Kim, H. S., Lee, Y. D., & Kim, H. S. (2008). Mesenchymal stem cells promote proliferation of endogenous neural stem cells and survival of newborn cells in a rat stroke model. Experimental & Molecular Medicine, 40, 387-397.
Yu, Q., Liu, L., Lin, J., Wang, Y., Xuan, X., Guo, Y., & Hu, S. (2015). SDF-1α/CXCR4 axis mediates the migration of mesenchymal stem cells to the hypoxic-ischemic brain lesion in a rat model. Cell Journal, 16, 440-447.
Zhang, R., Liu, Y., Yan, K., Chen, L., Chen, X. R., Li, P., Chen, F. F., & Jiang, X. D. (2013). Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. Journal of Neuroinflammation, 10, 106. https://doi.org/10.1186/1742-2094-10-106
Zibara, K., Ballout, N., Mondello, S., Karnib, N., Ramadan, N., Omais, S., Nabbouh, A., Caliz, D., Clavijo, A., Hu, Z., Ghanem, N., Gajavelli, S., & Kobeissy, F. (2019). Combination of drug and stem cells neurotherapy: Potential interventions in neurotrauma and traumatic brain injury. Neuropharmacology, 145(Pt B), 177-198. https://doi.org/10.1016/j.neuropharm.2018.09.032

Auteurs

Sushanta Kumar Mishra (S)

MRI Research Group, Institute of Nuclear Medicine and Allied Sciences (INMAS), DRDO, Delhi, India.
Division of Stem Cell and Gene Therapy Research, Institute of Nuclear Medicine and Allied Sciences (INMAS), DRDO, Delhi, India.

Subash Khushu (S)

MRI Research Group, Institute of Nuclear Medicine and Allied Sciences (INMAS), DRDO, Delhi, India.

Gurudutta Gangenahalli (G)

Division of Stem Cell and Gene Therapy Research, Institute of Nuclear Medicine and Allied Sciences (INMAS), DRDO, Delhi, India.

Classifications MeSH