Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

General Review Article

The Role of Stem Cells in the Therapy of Stroke

Author(s): Maria Ejma , Natalia Madetko , Anna Brzecka *, Piotr Alster , Sławomir Budrewicz , Magdalena Koszewicz, Marta Misiuk-Hojło, Irina K. Tomilova , Siva G. Somasundaram and Cecil E. Kirkland

Volume 20, Issue 3, 2022

Page: [630 - 647] Pages: 18

DOI: 10.2174/1570159X19666210806163352

Price: $65

Abstract

Background: Stroke is a major challenge in neurology due to its multifactorial genesis and irreversible consequences. Processes of endogenous post-stroke neurogenesis, although insufficient, may indicate possible direction of future therapy. Multiple research considers stem-cell-based approaches in order to maximize neuroregeneration and minimize post-stroke deficits.

Objective: Aim of this study is to review current literature considering post-stroke stem-cell- based therapy and possibilities of inducing neuroregeneration after brain vascular damage.

Methods: Papers included in this article were obtained from PubMed and MEDLINE databases. The following medical subject headings (MeSH) were used: “stem cell therapy”, “post-stroke neurogenesis”, “stem-cells stroke”, “stroke neurogenesis”, “stroke stem cells”, “stroke”, “cell therapy”, “neuroregeneration”, “neurogenesis”, “stem-cell human”, “cell therapy in human”. Ultimate inclusion was made after manual review of the obtained reference list.

Results: Attempts of stimulating neuroregeneration after stroke found in current literature include supporting endogenous neurogenesis, different routes of exogenous stem cells supplying and extracellular vesicles used as a method of particle transport.

Conclusion: Although further research in this field is required, post stroke brain recovery supported by exogenous stem cells seems to be promising future therapy revolutionizing modern neurology.

Keywords: Cell therapy, neurogenesis, stroke, stem-cells, extracellular vesicles, central nervous system.

Graphical Abstract
[1]
Tobin, M.K.; Stephen, T.K.L.; Lopez, K.L.; Pergande, M.R.; Bartholomew, A.M.; Cologna, S.M.; Lazarov, O. Activated mesenchymal stem cells induce recovery following stroke via regulation of inflammation and oligodendrogenesis. J. Am. Heart Assoc., 2020, 9(7)e013583
[http://dx.doi.org/10.1161/JAHA.119.013583] [PMID: 32204666]
[2]
Fan, B.; Pan, W.; Wang, X.; Wei, M.; He, A.; Zhao, A.; Chopp, M.; Zhang, Z.G.; Liu, X.S. Long noncoding RNA mediates stroke-induced neurogenesis. Stem Cells, 2020, 38(8), 973-985.
[http://dx.doi.org/10.1002/stem.3189] [PMID: 32346940]
[3]
Toda, T.; Gage, F.H. Review: Adult neurogenesis contributes to hippocampal plasticity. Cell Tissue Res., 2018, 373(3), 693-709.
[http://dx.doi.org/10.1007/s00441-017-2735-4] [PMID: 29185071]
[4]
Tonchev, A.B. Brain ischemia, neurogenesis, and neurotrophic receptor expression in primates. Arch. Ital. Biol., 2011, 149(2), 225-231.
[PMID: 21701994]
[5]
Curtis, M.A.; Kam, M.; Nannmark, U.; Anderson, M.F.; Axell, M.Z.; Wikkelso, C.; Holtås, S.; van Roon-Mom, W.M.; Björk-Eriksson, T.; Nordborg, C.; Frisén, J.; Dragunow, M.; Faull, R.L.; Eriksson, P.S. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science, 2007, 315(5816), 1243-1249.
[http://dx.doi.org/10.1126/science.1136281] [PMID: 17303719]
[6]
Ming, G.L.; Song, H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci., 2005, 28, 223-250.
[http://dx.doi.org/10.1146/annurev.neuro.28.051804.101459] [PMID: 16022595]
[7]
Stępień, T.; Tarka, S.; Chutorański, D.; Felczak, P.; Acewicz, A.; Wierzba-Bobrowicz, T. Neurogenesis in adult human brain after hemorrhage and ischemic stroke. Folia Neuropathol., 2018, 56(4), 293-300.
[http://dx.doi.org/10.5114/fn.2018.80862] [PMID: 30786666]
[8]
Martí-Fàbregas, J.; Romaguera-Ros, M.; Gómez-Pinedo, U.; Martínez-Ramírez, S.; Jiménez-Xarrié, E.; Marín, R.; Martí-Vilalta, J-L.; García-Verdugo, J-M. Proliferation in the human ipsilateral subventricular zone after ischemic stroke. Neurology, 2010, 74(5), 357-365.
[http://dx.doi.org/10.1212/WNL.0b013e3181cbccec] [PMID: 20054008]
[9]
Esteban-Garcia, N.; Nombela, C.; Garrosa, J.; Rascón-Ramirez, F.J.; Barcia, J.A.; Sánchez-Sánchez-Rojas, L. Neurorestoration approach by biomaterials in ischemic stroke. Front. Neurosci., 2020, 14, 431.
[http://dx.doi.org/10.3389/fnins.2020.00431] [PMID: 32477053]
[10]
Huang, L.; Zhang, L. Neural stem cell therapies and hypoxic-ischemic brain injury. Prog. Neurobiol., 2019, 173, 1-17.
[http://dx.doi.org/10.1016/j.pneurobio.2018.05.004] [PMID: 29758244]
[11]
Hermann, D.M.; Peruzzotti-Jametti, L.; Schlechter, J.; Bernstock, J.D.; Doeppner, T.R.; Pluchino, S. Neural precursor cells in the ischemic brain - integration, cellular crosstalk, and consequences for stroke recovery. Front. Cell. Neurosci., 2014, 8, 291.
[http://dx.doi.org/10.3389/fncel.2014.00291] [PMID: 25278840]
[12]
Zhang, R.L.; Chopp, M.; Roberts, C.; Liu, X.; Wei, M.; Nejad-Davarani, S.P.; Wang, X.; Zhang, Z.G. Stroke increases neural stem cells and angiogenesis in the neurogenic niche of the adult mouse. PLoS One, 2014, 9(12)e113972
[http://dx.doi.org/10.1371/journal.pone.0113972] [PMID: 25437857]
[13]
Marques, B.L.; Carvalho, G.A.; Freitas, E.M.M.; Chiareli, R.A.; Barbosa, T.G.; Di Araújo, A.G.P.; Nogueira, Y.L.; Ribeiro, R.I.; Parreira, R.C.; Vieira, M.S.; Resende, R.R.; Gomez, R.S.; Oliveira-Lima, O.C.; Pinto, M.C.X. The role of neurogenesis in neurorepair after ischemic stroke. Semin. Cell Dev. Biol., 2019, 95, 98-110.
[http://dx.doi.org/10.1016/j.semcdb.2018.12.003] [PMID: 30550812]
[14]
Zhu, S.Z.; Szeto, V.; Bao, M.H.; Sun, H.S.; Feng, Z.P. Pharmacological approaches promoting stem cell-based therapy following ischemic stroke insults. Acta Pharmacol. Sin., 2018, 39(5), 695-712.
[http://dx.doi.org/10.1038/aps.2018.23] [PMID: 29671416]
[15]
Crouch, E.E.; Liu, C.; Silva-Vargas, V.; Doetsch, F. Regional and stage-specific effects of prospectively purified vascular cells on the adult V-SVZ neural stem cell lineage. J. Neurosci., 2015, 35(11), 4528-4539.
[http://dx.doi.org/10.1523/JNEUROSCI.1188-14.2015] [PMID: 25788671]
[16]
Song, J.; Zhong, C.; Bonaguidi, M.A.; Sun, G.J.; Hsu, D.; Gu, Y.; Meletis, K.; Huang, Z.J.; Ge, S.; Enikolopov, G.; Deisseroth, K.; Luscher, B.; Christian, K.M.; Ming, G.L.; Song, H. Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature, 2012, 489(7414), 150-154.
[http://dx.doi.org/10.1038/nature11306] [PMID: 22842902]
[17]
Yu, Z.; Chen, L.F.; Tang, L.; Hu, C.L. Effects of recombinant adenovirus-mediated hypoxia-inducible factor-1alpha gene on proliferation and differentiation of endogenous neural stem cells in rats following intracerebral hemorrhage. Asian Pac. J. Trop. Med., 2013, 6(10), 762-767.
[http://dx.doi.org/10.1016/S1995-7645(13)60134-0] [PMID: 23870462]
[18]
Andres, R.H.; Choi, R.; Pendharkar, A.V.; Gaeta, X.; Wang, N.; Nathan, J.K.; Chua, J.Y.; Lee, S.W.; Palmer, T.D.; Steinberg, G.K.; Guzman, R. The CCR2/CCL2 interaction mediates the transendothelial recruitment of intravascularly delivered neural stem cells to the ischemic brain. Stroke, 2011, 42(10), 2923-2931.
[http://dx.doi.org/10.1161/STROKEAHA.110.606368] [PMID: 21836091]
[19]
Nakata, M.; Nakagomi, T.; Maeda, M.; Nakano-Doi, A.; Momota, Y.; Matsuyama, T. Induction of perivascular neural stem cells and possible contribution to neurogenesis following transient brain ischemia/reperfusion injury. Transl. Stroke Res., 2017, 8(2), 131-143.
[http://dx.doi.org/10.1007/s12975-016-0479-1] [PMID: 27352866]
[20]
Sims, N.R.; Yew, W.P. Reactive astrogliosis in stroke: Contributions of astrocytes to recovery of neurological function. Neurochem. Int., 2017, 107, 88-103.
[http://dx.doi.org/10.1016/j.neuint.2016.12.016] [PMID: 28057555]
[21]
Cabezas, R.; Avila-Rodriguez, M.; Vega-Vela, N.E.; Echeverria, V.; González, J.; Hidalgo, O.A.; Santos, A.B.; Aliev, G.; Barreto, G.E. Growth factors and astrocytes metabolism: Possible roles for platelet derived growth factor. Med. Chem., 2016, 12(3), 204-210.
[http://dx.doi.org/10.2174/1573406411666151019120444] [PMID: 26477707]
[22]
Rosenblum, S.; Smith, T.N.; Wang, N.; Chua, J.Y.; Westbroek, E.; Wang, K.; Guzman, R. BDNF pretreatment of human embryonic-derived neural stem cells improves cell survival and functional recovery after transplantation in hypoxic-ischemic stroke. Cell Transplant., 2015, 24(12), 2449-2461.
[http://dx.doi.org/10.3727/096368914X679354] [PMID: 24594369]
[23]
Becerra-Calixto, A.; Cardona-Gómez, G.P. The role of astrocytes in neuroprotection after brain stroke: Potential in cell therapy. Front. Mol. Neurosci., 2017, 10, 88.
[http://dx.doi.org/10.3389/fnmol.2017.00088] [PMID: 28420961]
[24]
Duan, C.L.; Liu, C.W.; Shen, S.W.; Yu, Z.; Mo, J.L.; Chen, X.H.; Sun, F.Y. Striatal astrocytes transdifferentiate into functional mature neurons following ischemic brain injury. Glia, 2015, 63(9), 1660-1670.
[http://dx.doi.org/10.1002/glia.22837] [PMID: 26031629]
[25]
Gonzalez-Perez, O.; Quiñones-Hinojosa, A. Astrocytes as neural stem cells in the adult brain. J. Stem Cells, 2012, 7(3), 181-188.
[PMID: 23619383]
[26]
Doetsch, F. The glial identity of neural stem cells. Nat. Neurosci., 2003, 6(11), 1127-1134.
[http://dx.doi.org/10.1038/nn1144] [PMID: 14583753]
[27]
Jiang, C.T.; Wu, W.F.; Deng, Y.H.; Ge, J.W. Modulators of microglia activation and polarization in ischemic stroke. Mol. Med. Rep., 2020, 21(5), 2006-2018.
[http://dx.doi.org/10.3892/mmr.2020.11003] [PMID: 32323760]
[28]
Xiong, X.Y.; Liu, L.; Yang, Q.W. Functions and mechanisms of microglia/macrophages in neuroinflammation and neurogenesis after stroke. Prog. Neurobiol., 2016, 142, 23-44.
[http://dx.doi.org/10.1016/j.pneurobio.2016.05.001] [PMID: 27166859]
[29]
Liu, R.; Diao, J.; He, S.; Li, B.; Fei, Y.; Li, Y.; Fang, W. XQ-1H protects against ischemic stroke by regulating microglia polarization through PPARγ pathway in mice. Int. Immunopharmacol., 2018, 57, 72-81.
[http://dx.doi.org/10.1016/j.intimp.2018.02.014] [PMID: 29475098]
[30]
Xu, R.; Li, X.; Boreland, A.J.; Posyton, A.; Kwan, K.; Hart, R.P.; Jiang, P. Human iPSC-derived mature microglia retain their identity and functionally integrate in the chimeric mouse brain. Nat. Commun., 2020, 11(1), 1577.
[http://dx.doi.org/10.1038/s41467-020-15411-9] [PMID: 32221280]
[31]
Ohab, J.J.; Fleming, S.; Blesch, A.; Carmichael, S.T. A neurovascular niche for neurogenesis after stroke. J. Neurosci., 2006, 26(50), 13007-13016.
[http://dx.doi.org/10.1523/JNEUROSCI.4323-06.2006] [PMID: 17167090]
[32]
Arvidsson, A.; Collin, T.; Kirik, D.; Kokaia, Z.; Lindvall, O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med., 2002, 8(9), 963-970.
[http://dx.doi.org/10.1038/nm747] [PMID: 12161747]
[33]
Liu, H.S.; Shen, H.; Luo, Y.; Hoffer, B.J.; Wang, Y.; Yang, Y. Post-treatment with cocaine- and amphetamine-regulated transcript enhances infarct resolution, reinnervation, and angiogenesis in stroke rats - an MRI study. NMR Biomed., 2016, 29(3), 361-370.
[http://dx.doi.org/10.1002/nbm.3461] [PMID: 26915794]
[34]
Wu, K.J.; Yu, S.; Lee, J.Y.; Hoffer, B.; Wang, Y. Improving neurorepair in stroke brain through endogenous neurogenesis-enhancing drugs. Cell Transplant., 2017, 26(9), 1596-1600.
[http://dx.doi.org/10.1177/0963689717721230] [PMID: 29113469]
[35]
Zhang, G.L.; Zhu, Z.H.; Wang, Y.Z. Neural stem cell transplantation therapy for brain ischemic stroke: review and perspectives. World J. Stem Cells, 2019, 11(10), 817-830.
[http://dx.doi.org/10.4252/wjsc.v11.i10.817] [PMID: 31692854]
[36]
Klein, R.; Mahlberg, N.; Ohren, M.; Ladwig, A.; Neumaier, B.; Graf, R.; Hoehn, M.; Albrechtsen, M.; Rees, S.; Fink, G.R.; Rueger, M.A.; Schroeter, M. The neural cell adhesion molecule-derived (ncam)-peptide fg loop (fgl) mobilizes endogenous neural stem cells and promotes endogenous regenerative capacity after stroke. J. Neuroimmune Pharmacol., 2016, 11(4), 708-720.
[http://dx.doi.org/10.1007/s11481-016-9694-5] [PMID: 27352075]
[37]
Meng, C.; Zhang, J.C.; Shi, R.L.; Zhang, S.H.; Yuan, S.Y. Inhibition of interleukin-6 abolishes the promoting effects of pair housing on post-stroke neurogenesis. Neuroscience, 2015, 307, 160-170.
[http://dx.doi.org/10.1016/j.neuroscience.2015.08.055] [PMID: 26327363]
[38]
Shang, K.; He, J.; Zou, J.; Qin, C.; Lin, L.; Zhou, L.Q.; Yang, L.L.; Wu, L.J.; Wang, W.; Zhan, K.B.; Tian, D.S. Fingolimod promotes angiogenesis and attenuates ischemic brain damage via modulating microglial polarization. Brain Res., 2020, 1726146509
[http://dx.doi.org/10.1016/j.brainres.2019.146509] [PMID: 31626784]
[39]
Jeong, J.H.; Kang, S.H.; Kim, D.K.; Lee, N.S.; Jeong, Y.G.; Han, S.Y. Protective effect of cholic acid-coated Poly Lactic-Co-Glycolic Acid (PLGA) nanoparticles loaded with erythropoietin on experimental stroke. J. Nanosci. Nanotechnol., 2019, 19(10), 6524-6533.
[http://dx.doi.org/10.1166/jnn.2019.17078] [PMID: 31026988]
[40]
Cui, W.; Liu, R.; Jin, H.; Huang, Y.; Liu, W.; He, M. The protective effect of polyethylene glycol-conjugated urokinase nanogels in rat models of ischemic stroke when administrated outside the usual time window. Biochem. Biophys. Res. Commun., 2020, 523(4), 887-893.
[http://dx.doi.org/10.1016/j.bbrc.2020.01.032] [PMID: 31955887]
[41]
Li, M.; Li, J.; Chen, J.; Liu, Y.; Cheng, X.; Yang, F.; Gu, N. Platelet membrane biomimetic magnetic nanocarriers for targeted delivery and in situ generation of nitric oxide in early ischemic stroke. ACS Nano, 2020, 14(2), 2024-2035.
[http://dx.doi.org/10.1021/acsnano.9b08587] [PMID: 31927980]
[42]
Balasubramanian, V.; Domanskyi, A.; Renko, J.M.; Sarparanta, M.; Wang, C.F.; Correia, A.; Mäkilä, E.; Alanen, O.S.; Salonen, J.; Airaksinen, A.J.; Tuominen, R.; Hirvonen, J.; Airavaara, M.; Santos, H.A. Engineered antibody-functionalized porous silicon nanoparticles for therapeutic targeting of pro-survival pathway in endogenous neuroblasts after stroke. Biomaterials, 2020, 227119556
[http://dx.doi.org/10.1016/j.biomaterials.2019.119556] [PMID: 31670035]
[43]
Tuladhar, A.; Obermeyer, J.M.; Payne, S.L.; Siu, R.C.W.; Zand, S.; Morshead, C.M.; Shoichet, M.S. Injectable hydrogel enables local and sustained co-delivery to the brain: two clinically approved biomolecules, cyclosporine and erythropoietin, accelerate functional recovery in rat model of stroke. Biomaterials, 2020, 235119794
[http://dx.doi.org/10.1016/j.biomaterials.2020.119794] [PMID: 31981761]
[44]
Ho, M.T.; Teal, C.J.; Shoichet, M.S. A hyaluronan/methylcellulose-based hydrogel for local cell and biomolecule delivery to the central nervous system. Brain Res. Bull., 2019, 148, 46-54.
[http://dx.doi.org/10.1016/j.brainresbull.2019.03.005] [PMID: 30898580]
[45]
Caicco, M.J.; Cooke, M.J.; Wang, Y.; Tuladhar, A.; Morshead, C.M.; Shoichet, M.S. A hydrogel composite system for sustained epi-cortical delivery of Cyclosporin A to the brain for treatment of stroke. J. Control. Release, 2013, 166(3), 197-202.
[http://dx.doi.org/10.1016/j.jconrel.2013.01.002] [PMID: 23306024]
[46]
Fernández-García, L.; Pérez-Rigueiro, J.; Martinez-Murillo, R.; Panetsos, F.; Ramos, M.; Guinea, G.V.; González-Nieto, D. Cortical reshaping and functional recovery induced by silk fibroin hydrogels-encapsulated stem cells implanted in stroke animals. Front. Cell. Neurosci., 2018, 12, 296.
[http://dx.doi.org/10.3389/fncel.2018.00296] [PMID: 30237762]
[47]
Sanchez-Rojas, L.; Gómez-Pinedo, U.; Benito-Martin, M.S.; León-Espinosa, G.; Rascón-Ramirez, F.; Lendinez, C.; Martínez-Ramos, C.; Matías-Guiu, J.; Pradas, M.M.; Barcia, J.A. Biohybrids of scaffolding hyaluronic acid biomaterials plus adipose stem cells home local neural stem and endothelial cells: implications for reconstruction of brain lesions after stroke. J. Biomed. Mater. Res. B Appl. Biomater., 2019, 107(5), 1598-1606.
[http://dx.doi.org/10.1002/jbm.b.34252] [PMID: 30307108]
[48]
Ju, R.; Wen, Y.; Gou, R.; Wang, Y.; Xu, Q. The experimental therapy on brain ischemia by improvement of local angiogenesis with tissue engineering in the mouse. Cell Transplant., 2014, 23(Suppl. 1), S83-S95.
[http://dx.doi.org/10.3727/096368914X684998] [PMID: 25302948]
[49]
Sato, Y.; Nakanishi, K.; Hayakawa, M.; Kakizawa, H.; Saito, A.; Kuroda, Y.; Ida, M.; Tokita, Y.; Aono, S.; Matsui, F.; Kojima, S.; Oohira, A. Reduction of brain injury in neonatal hypoxic-ischemic rats by intracerebroventricular injection of neural stem/progenitor cells together with chondroitinase ABC. Reprod. Sci., 2008, 15(6), 613-620.
[http://dx.doi.org/10.1177/1933719108317299] [PMID: 18579850]
[50]
Gao, L.; Xu, W.; Li, T.; Chen, J.; Shao, A.; Yan, F.; Chen, G. Stem cell therapy: a promising therapeutic method for intracerebral hemorrhage. Cell Transplant., 2018, 27(12), 1809-1824.
[http://dx.doi.org/10.1177/0963689718773363] [PMID: 29871521]
[51]
Nonaka, M.; Yoshikawa, M.; Nishimura, F.; Yokota, H.; Kimura, H.; Hirabayashi, H.; Nakase, H.; Ishizaka, S.; Wanaka, A.; Sakaki, T. Intraventricular transplantation of embryonic stem cell-derived neural stem cells in intracerebral hemorrhage rats. Neurol. Res., 2004, 26(3), 265-272.
[http://dx.doi.org/10.1179/016164104225014049] [PMID: 15142318]
[52]
Marei, H.E.; Hasan, A.; Rizzi, R.; Althani, A.; Afifi, N.; Cenciarelli, C.; Caceci, T.; Shuaib, A. Potential of stem cell-based therapy for ischemic stroke. Front. Neurol., 2018, 9, 34.
[http://dx.doi.org/10.3389/fneur.2018.00034] [PMID: 29467713]
[53]
Courties, G.; Herisson, F.; Sager, H.B.; Heidt, T.; Ye, Y.; Wei, Y.; Sun, Y.; Severe, N.; Dutta, P.; Scharff, J.; Scadden, D.T.; Weissleder, R.; Swirski, F.K.; Moskowitz, M.A.; Nahrendorf, M. Ischemic stroke activates hematopoietic bone marrow stem cells. Circ. Res., 2015, 116(3), 407-417.
[http://dx.doi.org/10.1161/CIRCRESAHA.116.305207] [PMID: 25362208]
[54]
Joshi, S.; Wollenzien, H.; Leclerc, E.; Jarajapu, Y.P. Hypoxic regulation of angiotensin-converting enzyme 2 and Mas receptor in human CD34+ cells. J. Cell. Physiol., 2019, 234(11), 20420-20431.
[http://dx.doi.org/10.1002/jcp.28643] [PMID: 30989646]
[55]
Barlow, S.; Brooke, G.; Chatterjee, K.; Price, G.; Pelekanos, R.; Rossetti, T.; Doody, M.; Venter, D.; Pain, S.; Gilshenan, K.; Atkinson, K. Comparison of human placenta- and bone marrow-derived multipotent mesenchymal stem cells. Stem Cells Dev., 2008, 17(6), 1095-1107.
[http://dx.doi.org/10.1089/scd.2007.0154] [PMID: 19006451]
[56]
Russell, A.L.; Lefavor, R.; Durand, N.; Glover, L.; Zubair, A.C. Modifiers of mesenchymal stem cell quantity and quality. Transfusion, 2018, 58(6), 1434-1440.
[http://dx.doi.org/10.1111/trf.14597] [PMID: 29582436]
[57]
Chrostek, M.R.; Fellows, E.G.; Crane, A.T.; Grande, A.W.; Low, W.C. Efficacy of stem cell-based therapies for stroke. Brain Res., 2019, 1722146362
[http://dx.doi.org/10.1016/j.brainres.2019.146362] [PMID: 31381876]
[58]
Qu, R.; Li, Y.; Gao, Q.; Shen, L.; Zhang, J.; Liu, Z.; Chen, X.; Chopp, M. Neurotrophic and growth factor gene expression profiling of mouse bone marrow stromal cells induced by ischemic brain extracts. Neuropathology, 2007, 27(4), 355-363.
[http://dx.doi.org/10.1111/j.1440-1789.2007.00792.x] [PMID: 17899689]
[59]
Chen, J.; Tang, Y.X.; Liu, Y.M.; Chen, J.; Hu, X.Q.; Liu, N.; Wang, S.X.; Zhang, Y.; Zeng, W.G.; Ni, H.J.; Zhao, B.; Chen, Y.F.; Tang, Z.P. Transplantation of adipose-derived stem cells is associated with neural differentiation and functional improvement in a rat model of intracerebral hemorrhage. CNS Neurosci. Ther., 2012, 18(10), 847-854.
[http://dx.doi.org/10.1111/j.1755-5949.2012.00382.x] [PMID: 22934896]
[60]
Gómez-Pinedo, U.; Sanchez-Rojas, L.; Benito-Martin, M.S.; Lendinez, C.; León-Espinosa, G.; Rascón-Ramirez, F.J.; Herrero, J.; Castro, B.; Moreno-Jiménez, L.; Del Olmo, M.; Matias-Guiu, J.A.; Matias-Guiu, J.; Barcia, J.A. Evaluation of the safety and efficacy of the therapeutic potential of adipose-derived stem cells injected in the cerebral ischemic penumbra. J. Stroke Cerebrovasc. Dis., 2018, 27(9), 2453-2465.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2018.05.001] [PMID: 30029838]
[61]
Mora-Lee, S.; Sirerol-Piquer, M.S.; Gutiérrez-Pérez, M.; Gomez-Pinedo, U.; Roobrouck, V.D.; López, T.; Casado-Nieto, M.; Abizanda, G.; Rabena, M.T.; Verfaille, C.; Prósper, F.; García-Verdugo, J.M.; Nait-Oumesmar, B. Therapeutic effects of HMAPC and hmsc transplantation after stroke in mice. PLoS One, 2012, 7(8)e43683
[http://dx.doi.org/10.1371/journal.pone.0043683]
[62]
Tsang, K.S.; Ng, C.P.S.; Zhu, X.L.; Wong, G.K.C.; Lu, G.; Ahuja, A.T.; Wong, K.S.L.; Ng, H.K.; Poon, W.S. Phase I/II randomized controlled trial of autologous bone marrow-derived mesenchymal stem cell therapy for chronic stroke. World J. Stem Cells, 2017, 9(8), 133-143.
[http://dx.doi.org/10.4252/wjsc.v9.i8.133] [PMID: 28928910]
[63]
Glicksman, M.A. Induced pluripotent stem cells: the most versatile source for stem cell therapy. Clin. Ther., 2018, 40(7), 1060-1065.
[http://dx.doi.org/10.1016/j.clinthera.2018.06.004] [PMID: 30049501]
[64]
Ortuño-Costela, M.D.C.; Cerrada, V.; García-López, M.; Gallardo, M.E. The Challenge of Bringing iPSCs to the Patient. Int. J. Mol. Sci., 2019, 20(24), 6305.
[http://dx.doi.org/10.3390/ijms20246305] [PMID: 31847153]
[65]
Oh, S.H.; Jeong, Y.W.; Choi, W.; Noh, J.E.; Lee, S.; Kim, H.S.; Song, J. Multimodal therapeutic effects of neural precursor cells derived from human-induced pluripotent stem cells through episomal plasmid-based reprogramming in a rodent model of ischemic stroke. Stem Cells Int., 2020, 20204061516
[http://dx.doi.org/10.1155/2020/4061516] [PMID: 32269595]
[66]
Vonderwalde, I.; Azimi, A.; Rolvink, G.; Ahlfors, J.E.; Shoichet, M.S.; Morshead, C.M. Transplantation of directly reprogrammed human neural precursor cells following stroke promotes synaptogenesis and functional recovery. Transl. Stroke Res., 2020, 11(1), 93-107.
[http://dx.doi.org/10.1007/s12975-019-0691-x] [PMID: 30747366]
[67]
Korshunova, I.; Rhein, S.; García-González, D.; Stölting, I.; Pfisterer, U.; Barta, A.; Dmytriyeva, O.; Kirkeby, A.; Schwaninger, M.; Khodosevich, K. Genetic modification increases the survival and the neuroregenerative properties of transplanted neural stem cells. JCI Insight, 2020, 5(4)e126268
[http://dx.doi.org/10.1172/jci.insight.126268] [PMID: 31999645]
[68]
Doeppner, T.R.; Ewert, T.A.; Tönges, L.; Herz, J.; Zechariah, A.; ElAli, A.; Ludwig, A.K.; Giebel, B.; Nagel, F.; Dietz, G.P.H.; Weise, J.; Hermann, D.M.; Bähr, M. Transduction of neural precursor cells with TAT-heat shock protein 70 chaperone: therapeutic potential against ischemic stroke after intrastriatal and systemic transplantation. Stem Cells, 2012, 30(6), 1297-1310.
[http://dx.doi.org/10.1002/stem.1098] [PMID: 22593021]
[69]
Lee, H.J.; Lim, I.J.; Lee, M.C.; Kim, S.U. Human neural stem cells genetically modified to overexpress brain-derived neurotrophic factor promote functional recovery and neuroprotection in a mouse stroke model. J. Neurosci. Res., 2010, 88(15), 3282-3294.
[http://dx.doi.org/10.1002/jnr.22474] [PMID: 20818776]
[70]
Lee, H.J.; Kim, K.S.; Park, I.H.; Kim, S.U. Human neural stem cells over-expressing VEGF provide neuroprotection, angiogenesis and functional recovery in mouse stroke model. PLoS One, 2007, 2(1)e156
[http://dx.doi.org/10.1371/journal.pone.0000156] [PMID: 17225860]
[71]
Chang, D.J.; Lee, N.; Choi, C.; Jeon, I.; Oh, S.H.; Shin, D.A.; Hwang, T.S.; Lee, H.J.; Kim, S.U.; Moon, H.; Hong, K.S.; Kang, K.S.; Song, J. Therapeutic effect of BDNF-overexpressing human neural stem cells (HB1.F3.BDNF) in a rodent model of middle cerebral artery occlusion. Cell Transplant., 2013, 22(8), 1441-1452.
[http://dx.doi.org/10.3727/096368912X657323] [PMID: 23044072]
[72]
Yang, C.; Zhou, L.; Gao, X.; Chen, B.; Tu, J.; Sun, H.; Liu, X.; He, J.; Liu, J.; Yuan, Q. Neuroprotective effects of bone marrow stem cells overexpressing glial cell line-derived neurotrophic factor on rats with intracerebral hemorrhage and neurons exposed to hypoxia/reoxygenation. Neurosurgery, 2011, 68(3), 691-704.
[http://dx.doi.org/10.1227/NEU.0b013e3182098a8a] [PMID: 21311297]
[73]
Zhang, G.; Guo, X.; Chen, L.; Li, B.; Gu, B.; Wang, H.; Wu, G.; Kong, J.; Chen, W.; Yu, Y. Interferon-γ promotes neuronal repair by transplanted neural stem cells in ischemic rats. Stem Cells Dev., 2018, 27(5), 355-366.
[http://dx.doi.org/10.1089/scd.2017.0225] [PMID: 29298609]
[74]
Chen, B.; Gao, X.Q.; Yang, C.X.; Tan, S.K.; Sun, Z.L.; Yan, N.H.; Pang, Y.G.; Yuan, M.; Chen, G.J.; Xu, G.T.; Zhang, K.; Yuan, Q.L. Neuroprotective effect of grafting GDNF gene-modified neural stem cells on cerebral ischemia in rats. Brain Res., 2009, 1284, 1-11.
[http://dx.doi.org/10.1016/j.brainres.2009.05.100] [PMID: 19520066]
[75]
Bang, O.Y.; Kim, E.H. Mesenchymal stem cell-derived extracellular vesicle therapy for stroke: challenges and progress. Front. Neurol., 2019, 10, 211.
[http://dx.doi.org/10.3389/fneur.2019.00211] [PMID: 30915025]
[76]
Xin, H.; Li, Y.; Chopp, M. Exosomes/miRNAs as mediating cell-based therapy of stroke. Front. Cell. Neurosci., 2014, 8, 377.
[http://dx.doi.org/10.3389/fncel.2014.00377] [PMID: 25426026]
[77]
Kourembanas, S. Exosomes: vehicles of intercellular signaling, biomarkers, and vectors of cell therapy. Annu. Rev. Physiol., 2015, 77, 13-27.
[http://dx.doi.org/10.1146/annurev-physiol-021014-071641] [PMID: 25293529]
[78]
Xin, H.; Li, Y.; Liu, Z.; Wang, X.; Shang, X.; Cui, Y.; Zhang, Z.G.; Chopp, M. MiR-133b promotes neural plasticity and functional recovery after treatment of stroke with multipotent mesenchymal stromal cells in rats via transfer of exosome-enriched extracellular particles. Stem Cells, 2013, 31(12), 2737-2746.
[http://dx.doi.org/10.1002/stem.1409] [PMID: 23630198]
[79]
Xin, H.; Li, Y.; Cui, Y.; Yang, J.J.; Zhang, Z.G.; Chopp, M. Systemic administration of exosomes released from mesenchymal stromal cells promote functional recovery and neurovascular plasticity after stroke in rats. J. Cereb. Blood Flow Metab., 2013, 33(11), 1711-1715.
[http://dx.doi.org/10.1038/jcbfm.2013.152] [PMID: 23963371]
[80]
Singh, M.; Pandey, P.K.; Bhasin, A.; Padma, M.V.; Mohanty, S. Application of stem cells in stroke: A multifactorial approach. Front. Neurosci., 2020, 14, 473.
[http://dx.doi.org/10.3389/fnins.2020.00473] [PMID: 32581669]
[81]
Jiang, M.; Wang, H.; Jin, M.; Yang, X.; Ji, H.; Jiang, Y.; Zhang, H.; Wu, F.; Wu, G.; Lai, X.; Cai, L.; Hu, R.; Xu, L.; Li, L. Exosomes from mir-30d-5p-adscs reverse acute ischemic stroke-induced, autophagy-mediated brain injury by promoting m2 microglial/macrophage polarization. Cell. Physiol. Biochem., 2018, 47(2), 864-878.
[http://dx.doi.org/10.1159/000490078] [PMID: 29807362]
[82]
Nalamolu, K.R.; Venkatesh, I.; Mohandass, A.; Klopfenstein, J.D.; Pinson, D.M.; Wang, D.Z.; Veeravalli, K.K. Exosomes treatment mitigates ischemic brain damage but does not improve post-stroke neurological outcome. Cell. Physiol. Biochem., 2019, 52(6), 1280-1291.
[http://dx.doi.org/10.33594/000000090] [PMID: 31026391]
[83]
Zhou, S.; Gao, B.; Sun, C.; Bai, Y.; Cheng, D.; Zhang, Y.; Li, X.; Zhao, J.; Xu, D. Vascular endothelial cell-derived exosomes protect neural stem cells against ischemia/reperfusion injury. Neuroscience, 2020, 441, 184-196.
[http://dx.doi.org/10.1016/j.neuroscience.2020.05.046] [PMID: 32502570]
[84]
Otero-Ortega, L.; Gómez de Frutos, M.C.; Laso-García, F.; Rodríguez-Frutos, B.; Medina-Gutiérrez, E.; López, J.A.; Vázquez, J.; Díez-Tejedor, E.; Gutiérrez-Fernández, M. Exosomes promote restoration after an experimental animal model of intracerebral hemorrhage. J. Cereb. Blood Flow Metab., 2018, 38(5), 767-779.
[http://dx.doi.org/10.1177/0271678X17708917] [PMID: 28524762]
[85]
Reza-Zaldivar, E.E.; Hernández-Sapiéns, M.A.; Gutiérrez-Mercado, Y.K.; Sandoval-Ávila, S.; Gomez-Pinedo, U.; Márquez-Aguirre, A.L.; Vázquez-Méndez, E.; Padilla-Camberos, E.; Canales-Aguirre, A.A. Mesenchymal stem cell-derived exosomes promote neurogenesis and cognitive function recovery in a mouse model of Alzheimer’s disease. Neural Regen. Res., 2019, 14(9), 1626-1634.
[http://dx.doi.org/10.4103/1673-5374.255978] [PMID: 31089063]
[86]
Rodríguez-Frutos, B.; Otero-Ortega, L.; Gutiérrez-Fernández, M.; Fuentes, B.; Ramos-Cejudo, J.; Díez-Tejedor, E. Stem cell therapy and administration routes after stroke. Transl. Stroke Res., 2016, 7(5), 378-387.
[http://dx.doi.org/10.1007/s12975-016-0482-6] [PMID: 27384771]
[87]
Saraf, J.; Sarmah, D.; Vats, K.; Kaur, H.; Pravalika, K.; Wanve, M.; Kalia, K.; Borah, A.; Dave, K.R.; Yavagal, D.R.; Bhattacharya, P. Intra-arterial stem cell therapy modulates neuronal calcineurin and confers neuroprotection after ischemic stroke. Int. J. Neurosci., 2019, 129(10), 1039-1044.
[http://dx.doi.org/10.1080/00207454.2019.1633315] [PMID: 31203689]
[88]
Ashwal, S.; Ghosh, N.; Turenius, C.I.; Dulcich, M.; Denham, C.M.; Tone, B.; Hartman, R.; Snyder, E.Y.; Obenaus, A. Reparative effects of neural stem cells in neonatal rats with hypoxic-ischemic injury are not influenced by host sex. Pediatr. Res., 2014, 75(5), 603-611.
[http://dx.doi.org/10.1038/pr.2014.7] [PMID: 24463490]
[89]
Ji, G.; Liu, M.; Zhao, X.F.; Liu, X.Y.; Guo, Q.L.; Guan, Z.F.; Zhou, H.G.; Guo, J.C. NF-κB signaling is involved in the effects of intranasally engrafted human neural stem cells on neurofunctional improvements in neonatal rat hypoxic-ischemic encephalopathy. CNS Neurosci. Ther., 2015, 21(12), 926-935.
[http://dx.doi.org/10.1111/cns.12441] [PMID: 26255634]
[90]
Turnbull, M.T.; Zubair, A.C.; Meschia, J.F.; Freeman, W.D. Mesenchymal stem cells for hemorrhagic stroke: status of preclinical and clinical research. NPJ Regen. Med., 2019, 4, 10.
[http://dx.doi.org/10.1038/s41536-019-0073-8] [PMID: 31098299]
[91]
Kondori, B.J.; Asadi, M.H.; Bahadoran, H.; Yari, A.; Sarshoori, J.R. Intra-arterial transplantation of neural stem cells improve functional recovery after transient ischemic stroke in adult rats. Bratisl. Lek Listy, 2020, 121(1), 8-13.
[http://dx.doi.org/10.4149/BLL_2020_002] [PMID: 31950834]
[92]
Yu, S.P.; Tung, J.K.; Wei, Z.Z.; Chen, D.; Berglund, K.; Zhong, W.; Zhang, J.Y.; Gu, X.; Song, M.; Gross, R.E.; Lin, S.Z.; Wei, L. Optochemogenetic stimulation of transplanted IPS-NPCS enhances neuronal repair and functional recovery after ischemic stroke. J. Neurosci., 2019, 39(33), 6571-6594.
[http://dx.doi.org/10.1523/JNEUROSCI.2010-18.2019] [PMID: 31263065]
[93]
Satani, N.; Cai, C.; Giridhar, K.; McGhiey, D.; George, S.; Parsha, K.; Nghiem, D.M.; Valenzuela, K.S.; Riecke, J.; Vahidy, F.S.; Savitz, S.I. World-wide efficacy of bone marrow derived mesenchymal stromal cells in preclinical ischemic stroke models: Systematic review and meta-analysis. Front. Neurol., 2019, 10, 405.
[http://dx.doi.org/10.3389/fneur.2019.00405] [PMID: 31068894]
[94]
Lappalainen, R.S.; Narkilahti, S.; Huhtala, T.; Liimatainen, T.; Suuronen, T.; Närvänen, A.; Suuronen, R.; Hovatta, O.; Jolkkonen, J. The SPECT imaging shows the accumulation of neural progenitor cells into internal organs after systemic administration in middle cerebral artery occlusion rats. Neurosci. Lett., 2008, 440(3), 246-250.
[http://dx.doi.org/10.1016/j.neulet.2008.05.090] [PMID: 18572314]
[95]
Lee, S.T.; Chu, K.; Jung, K.H.; Kim, S.J.; Kim, D.H.; Kang, K.M.; Hong, N.H.; Kim, J.H.; Ban, J.J.; Park, H.K.; Kim, S.U.; Park, C.G.; Lee, S.K.; Kim, M.; Roh, J.K. Anti-inflammatory mechanism of intravascular neural stem cell transplantation in haemorrhagic stroke. Brain, 2008, 131(Pt 3), 616-629.
[http://dx.doi.org/10.1093/brain/awm306] [PMID: 18156155]
[96]
Yang, B.; Xi, X.; Aronowski, J.; Savitz, S.I. Ischemic stroke may activate bone marrow mononuclear cells to enhance recovery after stroke. Stem Cells Dev., 2012, 21(18), 3332-3340.
[http://dx.doi.org/10.1089/scd.2012.0037] [PMID: 22731389]
[97]
Vu, Q.; Xie, K.; Eckert, M.; Zhao, W.; Cramer, S.C. Meta-analysis of preclinical studies of mesenchymal stromal cells for ischemic stroke. Neurology, 2014, 82(14), 1277-1286.
[http://dx.doi.org/10.1212/WNL.0000000000000278] [PMID: 24610327]
[98]
Bacigaluppi, M.; Pluchino, S.; Peruzzotti-Jametti, L.; Kilic, E.; Kilic, U.; Salani, G.; Brambilla, E.; West, M.J.; Comi, G.; Martino, G.; Hermann, D.M. Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain, 2009, 132(Pt 8), 2239-2251.
[http://dx.doi.org/10.1093/brain/awp174] [PMID: 19617198]
[99]
Hao, L.; Zou, Z.; Tian, H.; Zhang, Y.; Zhou, H.; Liu, L. Stem cell-based therapies for ischemic stroke. BioMed Res. Int., 2014, 2014468748
[http://dx.doi.org/10.1155/2014/468748] [PMID: 24719869]
[100]
Chen, L.; Zhang, G.; Gu, Y.; Guo, X. Meta-analysis and systematic review of neural stem cells therapy for experimental ischemia stroke in preclinical studies. Sci. Rep., 2016, 6, 32291.
[http://dx.doi.org/10.1038/srep32291] [PMID: 27554433]
[101]
Darsalia, V.; Allison, S.J.; Cusulin, C.; Monni, E.; Kuzdas, D.; Kallur, T.; Lindvall, O.; Kokaia, Z. Cell number and timing of transplantation determine survival of human neural stem cell grafts in stroke-damaged rat brain. J. Cereb. Blood Flow Metab., 2011, 31(1), 235-242.
[http://dx.doi.org/10.1038/jcbfm.2010.81] [PMID: 20531461]
[102]
Janowski, M.; Lyczek, A.; Engels, C.; Xu, J.; Lukomska, B.; Bulte, J.W.; Walczak, P. Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J. Cereb. Blood Flow Metab., 2013, 33(6), 921-927.
[http://dx.doi.org/10.1038/jcbfm.2013.32] [PMID: 23486296]
[103]
Kondziolka, D.; Steinberg, G.K.; Wechsler, L.; Meltzer, C.C.; Elder, E.; Gebel, J.; Decesare, S.; Jovin, T.; Zafonte, R.; Lebowitz, J.; Flickinger, J.C.; Tong, D.; Marks, M.P.; Jamieson, C.; Luu, D.; Bell-Stephens, T.; Teraoka, J. Neurotransplantation for patients with subcortical motor stroke: a phase 2 randomized trial. J. Neurosurg., 2005, 103(1), 38-45.
[http://dx.doi.org/10.3171/jns.2005.103.1.0038] [PMID: 16121971]
[104]
Kondziolka, D.; Wechsler, L.; Goldstein, S.; Meltzer, C.; Thulborn, K.R.; Gebel, J.; Jannetta, P.; DeCesare, S.; Elder, E.M.; McGrogan, M.; Reitman, M.A.; Bynum, L. Transplantation of cultured human neuronal cells for patients with stroke. Neurology, 2000, 55(4), 565-569.
[http://dx.doi.org/10.1212/WNL.55.4.565] [PMID: 10953194]
[105]
Savitz, S.I.; Dinsmore, J.; Wu, J.; Henderson, G.V.; Stieg, P.; Caplan, L.R. Neurotransplantation of fetal porcine cells in patients with basal ganglia infarcts: a preliminary safety and feasibility study. Cerebrovasc. Dis., 2005, 20(2), 101-107.
[http://dx.doi.org/10.1159/000086518] [PMID: 15976503]
[106]
Kalladka, D.; Sinden, J.; Pollock, K.; Haig, C.; McLean, J.; Smith, W.; McConnachie, A.; Santosh, C.; Bath, P.M.; Dunn, L.; Muir, K.W. Human neural stem cells in patients with chronic ischaemic stroke (PISCES): a phase 1, first-in-man study. Lancet, 2016, 388(10046), 787-796.
[http://dx.doi.org/10.1016/S0140-6736(16)30513-X] [PMID: 27497862]
[107]
Conover, J.C.; Shook, B.A. Aging of the subventricular zone neural stem cell niche. Aging Dis., 2011, 2(1), 149-163.
[PMID: 22140636]
[108]
Jin, K.; Xie, L.; Mao, X.; Greenberg, M.B.; Moore, A.; Peng, B.; Greenberg, R.B.; Greenberg, D.A. Effect of human neural precursor cell transplantation on endogenous neurogenesis after focal cerebral ischemia in the rat. Brain Res., 2011, 1374, 56-62.
[http://dx.doi.org/10.1016/j.brainres.2010.12.037] [PMID: 21167824]
[109]
Jiang, Y.; Vaessen, B.; Lenvik, T.; Blackstad, M.; Reyes, M.; Verfaillie, C.M. Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp. Hematol., 2002, 30(8), 896-904.
[http://dx.doi.org/10.1016/S0301-472X(02)00869-X] [PMID: 12160841]
[110]
Díez-Tejedor, E.; Gutiérrez-Fernández, M.; Martínez-Sánchez, P.; Rodríguez-Frutos, B.; Ruiz-Ares, G.; Lara, M.L.; Gimeno, B.F. Reparative therapy for acute ischemic stroke with allogeneic mesenchymal stem cells from adipose tissue: a safety assessment: a phase II randomized, double-blind, placebo-controlled, single-center, pilot clinical trial. J. Stroke Cerebrovasc. Dis., 2014, 23(10), 2694-2700.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2014.06.011] [PMID: 25304723]
[111]
Hess, D.C.; Sila, C.A.; Furlan, A.J.; Wechsler, L.R.; Switzer, J.A.; Mays, R.W. A double-blind placebo-controlled clinical evaluation of MultiStem for the treatment of ischemic stroke. Int. J. Stroke, 2014, 9(3), 381-386.
[http://dx.doi.org/10.1111/ijs.12065] [PMID: 23692637]
[112]
Steinberg, G.K.; Kondziolka, D.; Wechsler, L.R.; Lunsford, L.D.; Coburn, M.L.; Billigen, J.B.; Kim, A.S.; Johnson, J.N.; Bates, D.; King, B.; Case, C.; McGrogan, M.; Yankee, E.W.; Schwartz, N.E. Clinical outcomes of transplanted modified bone marrow-derived mesenchymal stem cells in stroke: a phase 1/2a study. Stroke, 2016, 47(7), 1817-1824.
[http://dx.doi.org/10.1161/STROKEAHA.116.012995] [PMID: 27256670]
[113]
Lee, J.S.; Hong, J.M.; Moon, G.J.; Lee, P.H.; Ahn, Y.H.; Bang, O.Y. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells, 2010, 28(6), 1099-1106.
[http://dx.doi.org/10.1002/stem.430] [PMID: 20506226]
[114]
Prasad, K.; Sharma, A.; Garg, A.; Mohanty, S.; Bhatnagar, S.; Johri, S.; Singh, K.K.; Nair, V.; Sarkar, R.S.; Gorthi, S.P.; Hassan, K.M.; Prabhakar, S.; Marwaha, N.; Khandelwal, N.; Misra, U.K.; Kalita, J.; Nityanand, S.; Inve, S.T. Intravenous autologous bone marrow mononuclear stem cell therapy for ischemic stroke: a multicentric, randomized trial. Stroke, 2014, 45(12), 3618-3624.
[http://dx.doi.org/10.1161/STROKEAHA.114.007028] [PMID: 25378424]
[115]
Moniche, F.; Gonzalez, A.; Gonzalez-Marcos, J.R.; Carmona, M.; Piñero, P.; Espigado, I.; Garcia-Solis, D.; Cayuela, A.; Montaner, J.; Boada, C.; Rosell, A.; Jimenez, M.D.; Mayol, A.; Gil-Peralta, A. Intra-arterial bone marrow mononuclear cells in ischemic stroke: a pilot clinical trial. Stroke, 2012, 43(8), 2242-2244.
[http://dx.doi.org/10.1161/STROKEAHA.112.659409] [PMID: 22764211]
[116]
Prasad, K.; Mohanty, S.; Bhatia, R.; Srivastava, M.V.; Garg, A.; Srivastava, A.; Goyal, V.; Tripathi, M.; Kumar, A.; Bal, C.; Vij, A.; Mishra, N.K. Autologous intravenous bone marrow mononuclear cell therapy for patients with subacute ischaemic stroke: a pilot study. Indian J. Med. Res., 2012, 136(2), 221-228.
[PMID: 22960888]
[117]
Savitz, S.I.; Misra, V.; Kasam, M.; Juneja, H.; Cox, C.S., Jr; Alderman, S.; Aisiku, I.; Kar, S.; Gee, A.; Grotta, J.C. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann. Neurol., 2011, 70(1), 59-69.
[http://dx.doi.org/10.1002/ana.22458] [PMID: 21786299]
[118]
Oh, S.H.; Choi, C.; Chang, D.J.; Shin, D.A.; Lee, N.; Jeon, I.; Sung, J.H.; Lee, H.; Hong, K.S.; Ko, J.J.; Song, J. Early neuroprotective effect with lack of long-term cell replacement effect on experimental stroke after intra-arterial transplantation of adipose-derived mesenchymal stromal cells. Cytotherapy, 2015, 17(8), 1090-1103.
[http://dx.doi.org/10.1016/j.jcyt.2015.04.007] [PMID: 26031742]
[119]
Hsiao, S.T.F.; Asgari, A.; Lokmic, Z.; Sinclair, R.; Dusting, G.J.; Lim, S.Y.; Dilley, R.J. Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue. Stem Cells Dev., 2012, 21(12), 2189-2203.
[http://dx.doi.org/10.1089/scd.2011.0674] [PMID: 22188562]
[120]
Cunningham, C.J.; Redondo-Castro, E.; Allan, S.M. The therapeutic potential of the mesenchymal stem cell secretome in ischaemic stroke. J. Cereb. Blood Flow Metab., 2018, 38(8), 1276-1292.
[http://dx.doi.org/10.1177/0271678X18776802] [PMID: 29768965]
[121]
Liem, N.T.; Huyen, T.L.; Huong, L.T.; Doan, N.V.; Anh, B.V.; Anh, N.T.P.; Tung, D.T. Outcomes of bone marrow mononuclear cell transplantation for neurological sequelae due to intracranial hemorrhage incidence in the neonatal period: report of four cases. Front Pediatr., 2020, 7, 543.
[http://dx.doi.org/10.3389/fped.2019.00543] [PMID: 32039110]
[122]
Bedini, G.; Bersano, A.; Zanier, E.R.; Pischiutta, F.; Parati, E.A. Mesenchymal stem cell therapy in intracerebral haemorrhagic stroke. Curr. Med. Chem., 2018, 25(19), 2176-2197.
[http://dx.doi.org/10.2174/0929867325666180111101410] [PMID: 29332564]
[123]
Liu, W.; Li, R.; Yin, J.; Guo, S.; Chen, Y.; Fan, H.; Li, G.; Li, Z.; Li, X.; Zhang, X.; He, X.; Duan, C. Mesenchymal stem cells alleviate the early brain injury of subarachnoid hemorrhage partly by suppression of Notch1-dependent neuroinflammation: involvement of Botch. J. Neuroinflammation, 2019, 16(1), 8.
[http://dx.doi.org/10.1186/s12974-019-1396-5] [PMID: 30646897]
[124]
Gao, X.; Xiong, Y.; Li, Q.; Han, M.; Shan, D.; Yang, G.; Zhang, S.; Xin, D.; Zhao, R.; Wang, Z.; Xue, H.; Li, G. Extracellular vesicle-mediated transfer of miR-21-5p from mesenchymal stromal cells to neurons alleviates early brain injury to improve cognitive function via the PTEN/Akt pathway after subarachnoid hemorrhage. Cell Death Dis., 2020, 11(5), 363.
[http://dx.doi.org/10.1038/s41419-020-2530-0] [PMID: 32404916]
[125]
Li, Z.M.; Zhang, Z.T.; Guo, C.J.; Geng, F.Y.; Qiang, F.; Wang, L.X. Autologous bone marrow mononuclear cell implantation for intracerebral hemorrhage-a prospective clinical observation. Clin. Neurol. Neurosurg., 2013, 115(1), 72-76.
[http://dx.doi.org/10.1016/j.clineuro.2012.04.030] [PMID: 22657095]
[126]
Zhang, Q.; Shang, X.; Hao, M.; Zheng, M.; Li, Y.; Liang, Z.; Cui, Y.; Liu, Z. Effects of human umbilical cord mesenchymal stem cell transplantation combined with minimally invasive hematoma aspiration on intracerebral hemorrhage in rats. Am. J. Transl. Res., 2015, 7(11), 2176-2186.
[PMID: 26807166]
[127]
Lees, J.S.; Sena, E.S.; Egan, K.J.; Antonic, A.; Koblar, S.A.; Howells, D.W.; MacLeod, M.R. Stem cell-based therapy for experimental stroke: a systematic review and meta-analysis. Int. J. Stroke, 2012, 7(7), 582-588.
[http://dx.doi.org/10.1111/j.1747-4949.2012.00797.x] [PMID: 22687044]
[128]
Lalu, M.M.; McIntyre, L.; Pugliese, C.; Fergusson, D.; Winston, B.W.; Marshall, J.C.; Granton, J.; Stewart, D.J. Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One, 2012, 7(10)e47559
[http://dx.doi.org/10.1371/journal.pone.0047559] [PMID: 23133515]
[129]
Le Blanc, K.; Tammik, C.; Rosendahl, K.; Zetterberg, E.; Ringdén, O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp. Hematol., 2003, 31(10), 890-896.
[http://dx.doi.org/10.1016/S0301-472X(03)00110-3] [PMID: 14550804]
[130]
Lalu, M.M.; Montroy, J.; Dowlatshahi, D.; Hutton, B.; Juneau, P.; Wesch, N.; Zhang, S.Y.; McGinn, R.; Corbett, D.; Stewart, D.J.; Fergusson, D.A. From the lab to patients: A systematic review and meta-analysis of mesenchymal stem cell therapy for stroke. Transl. Stroke Res., 2020, 11, 345.
[http://dx.doi.org/10.1007/s12975-019-00736-5]
[131]
Zheng, H.; Zhang, B.; Chhatbar, P.Y.; Dong, Y.; Alawieh, A.; Lowe, F.; Hu, X.; Feng, W. Mesenchymal stem cell therapy in stroke: A systematic review of literature in pre-clinical and clinical research. Cell Transplant., 2018, 27(12), 1723-1730.
[http://dx.doi.org/10.1177/0963689718806846] [PMID: 30343609]
[132]
Tornero, D.; Tsupykov, O.; Granmo, M.; Rodriguez, C.; Grønning-Hansen, M.; Thelin, J.; Smozhanik, E.; Laterza, C.; Wattananit, S.; Ge, R.; Tatarishvili, J.; Grealish, S.; Brüstle, O.; Skibo, G.; Parmar, M.; Schouenborg, J.; Lindvall, O.; Kokaia, Z. Synaptic inputs from stroke-injured brain to grafted human stem cell-derived neurons activated by sensory stimuli. Brain, 2017, 140(3), 692-706.
[http://dx.doi.org/10.1093/brain/aww347] [PMID: 28115364]
[133]
Hermanto, Y.; Maki, T.; Takagi, Y.; Miyamoto, S.; Takahashi, J. Xeno-free culture for generation of forebrain oligodendrocyte precursor cells from human pluripotent stem cells. J. Neurosci. Res., 2019, 97(7), 828-845.
[http://dx.doi.org/10.1002/jnr.24413] [PMID: 30891830]
[134]
Liu, J.; Wang, Y.; Akamatsu, Y.; Lee, C.C.; Stetler, R.A.; Lawton, M.T.; Yang, G.Y. Vascular remodeling after ischemic stroke: mechanisms and therapeutic potentials. Prog. Neurobiol., 2014, 115, 138-156.
[http://dx.doi.org/10.1016/j.pneurobio.2013.11.004] [PMID: 24291532]
[135]
Bacigaluppi, M.; Russo, G.L.; Peruzzotti-Jametti, L.; Rossi, S.; Sandrone, S.; Butti, E.; De Ceglia, R.; Bergamaschi, A.; Motta, C.; Gallizioli, M.; Studer, V.; Colombo, E.; Farina, C.; Comi, G.; Politi, L.S.; Muzio, L.; Villani, C.; Invernizzi, R.W.; Hermann, D.M.; Centonze, D.; Martino, G. Neural stem cell transplantation induces stroke recovery by upregulating glutamate transporter glt-1 in astrocytes. J. Neurosci., 2016, 36(41), 10529-10544.
[http://dx.doi.org/10.1523/JNEUROSCI.1643-16.2016] [PMID: 27733606]
[136]
Caporarello, N.; D’Angeli, F.; Cambria, M.T.; Candido, S.; Giallongo, C.; Salmeri, M.; Lombardo, C.; Longo, A.; Giurdanella, G.; Anfuso, C.D.; Lupo, G. Pericytes in microvessels: From “mural” function to brain and retina regeneration. Int. J. Mol. Sci., 2019, 20(24), 6351.
[http://dx.doi.org/10.3390/ijms20246351] [PMID: 31861092]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy