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Current Neuropharmacology

Editor-in-Chief

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

Review Article

The Effects and Underlying Mechanisms of Cell Therapy on Blood-Brain Barrier Integrity After Ischemic Stroke

Author(s): Li Gao, Zhenghong Song, Jianhua Mi, Pinpin Hou, Chong Xie, Jianquan Shi, Yansheng Li* and Anatol Manaenko*

Volume 18, Issue 12, 2020

Page: [1213 - 1226] Pages: 14

DOI: 10.2174/1570159X18666200914162013

Price: $65

Abstract

Ischemic stroke is one of the main causes of mortality and disability worldwide. However, efficient therapeutic strategies are still lacking. Stem/progenitor cell-based therapy, with its vigorous advantages, has emerged as a promising tool for the treatment of ischemic stroke. The mechanisms involve new neural cells and neuronal circuitry formation, antioxidation, inflammation alleviation, angiogenesis, and neurogenesis promotion. In the past decades, in-depth studies have suggested that cell therapy could promote vascular stabilization and decrease blood-brain barrier (BBB) leakage after ischemic stroke. However, the effects and underlying mechanisms on BBB integrity induced by the engrafted cells in ischemic stroke have not been reviewed yet. Herein, we will update the progress in research on the effects of cell therapy on BBB integrity after ischemic stroke and review the underlying mechanisms. First, we will present an overview of BBB dysfunction under the ischemic condition and cells engraftment for ischemic treatment. Then, we will summarize and discuss the current knowledge about the effects and underlying mechanisms of cell therapy on BBB integrity after ischemic stroke. In particular, we will review the most recent studies in regard to the relationship between cell therapy and BBB in tissue plasminogen activator (t-PA)-mediated therapy and diabetic stroke.

Keywords: Ischemic stroke, stem cells, blood-brain barrier, tissue plasminogen activator, neurogenesis.

Graphical Abstract

[1]
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]
[2]
Sarmah, D.; Kaur, H.; Saraf, J.; Pravalika, K.; Goswami, A.; Kalia, K.; Borah, A.; Wang, X.; Dave, K.R.; Yavagal, D.R.; Bhattacharya, P. Getting closer to an effective intervention of ischemic stroke: the big promise of stem cell. Transl. Stroke Res., 2018, 9(4), 356-374.
[http://dx.doi.org/10.1007/s12975-017-0580-0] [PMID: 29075984]
[3]
Borlongan, C.V.; Lind, J.G.; Dillon-Carter, O.; Yu, G.; Hadman, M.; Cheng, C.; Carroll, J.; Hess, D.C. Bone marrow grafts restore cerebral blood flow and blood brain barrier in stroke rats. Brain Res., 2004, 1010(1-2), 108-116.
[http://dx.doi.org/10.1016/j.brainres.2004.02.072] [PMID: 15126123]
[4]
Zacharek, A.; Chen, J.; Cui, X.; Li, A.; Li, Y.; Roberts, C.; Feng, Y.; Gao, Q.; Chopp, M. Angiopoietin1/Tie2 and VEGF/Flk1 induced by MSC treatment amplifies angiogenesis and vascular stabilization after stroke. J. Cereb. Blood Flow Metab., 2007, 27(10), 1684-1691.
[http://dx.doi.org/10.1038/sj.jcbfm.9600475] [PMID: 17356562]
[5]
Lalu, M.M.; Montroy, J.; Dowlatshahi, D.; Hutton, B.; Juneau, P.; Wesch, N.; Zhang, Y. S.; McGinn, R.; Corbett, D.; Stewart, D.J.A.; A Fergusson, D. From the lab to patients: a systematic review and meta-analysis of mesenchymal stem cell therapy for stroke. Transl. Stroke Res., 2020, 11(3), 345-364.
[http://dx.doi.org/10.1007/s12975-019-00736-5] [PMID: 31654281]
[6]
Obermeier, B.; Daneman, R.; Ransohoff, R.M. Development, maintenance and disruption of the blood-brain barrier. Nat. Med., 2013, 19(12), 1584-1596.
[http://dx.doi.org/10.1038/nm.3407] [PMID: 24309662]
[7]
Abbott, N.J.; Patabendige, A.A.; Dolman, D.E.; Yusof, S.R.; Begley, D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis., 2010, 37(1), 13-25.
[http://dx.doi.org/10.1016/j.nbd.2009.07.030] [PMID: 19664713]
[8]
Saunders, N.R.; Liddelow, S.A.; Dziegielewska, K.M. Barrier mechanisms in the developing brain. Front. Pharmacol., 2012, 3, 46.
[http://dx.doi.org/10.3389/fphar.2012.00046] [PMID: 22479246]
[9]
Keaney, J.; Campbell, M. The dynamic blood-brain barrier. FEBS J., 2015, 282(21), 4067-4079.
[http://dx.doi.org/10.1111/febs.13412] [PMID: 26277326]
[10]
Shepro, D.; Morel, N.M. Pericyte physiology. FASEB J., 1993, 7(11), 1031-1038.
[http://dx.doi.org/10.1096/fasebj.7.11.8370472] [PMID: 8370472]
[11]
Daneman, R.; Prat, A. The blood-brain barrier. Cold Spring Harb. Perspect. Biol., 2015, 7(1), a020412.
[http://dx.doi.org/10.1101/cshperspect.a020412] [PMID: 25561720]
[12]
Armulik, A.; Genové, G.; Betsholtz, C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell, 2011, 21(2), 193-215.
[http://dx.doi.org/10.1016/j.devcel.2011.07.001] [PMID: 21839917]
[13]
Siracusa, R.; Fusco, R.; Cuzzocrea, S. Astrocytes: role and functions in brain pathologies. Front. Pharmacol., 2019, 10, 1114.
[http://dx.doi.org/10.3389/fphar.2019.01114] [PMID: 31611796]
[14]
Narayanan, S.V.; Dave, K.R.; Perez-Pinzon, M.A. Ischemic preconditioning protects astrocytes against oxygen glucose deprivation via the nuclear erythroid 2-related factor 2 pathway. Transl. Stroke Res., 2018, 9(2), 99-109.
[http://dx.doi.org/10.1007/s12975-017-0574-y] [PMID: 29103101]
[15]
Mäe, M.; Armulik, A.; Betsholtz, C. Getting to know the cast - cellular interactions and signaling at the neurovascular unit. Curr. Pharm. Des., 2011, 17(26), 2750-2754.
[http://dx.doi.org/10.2174/138161211797440113] [PMID: 21827409]
[16]
Muoio, V.; Persson, P.B.; Sendeski, M.M. The neurovascular unit - concept review. Acta Physiol. (Oxf.), 2014, 210(4), 790-798.
[http://dx.doi.org/10.1111/apha.12250] [PMID: 24629161]
[17]
Steliga A.; Kowiański, P.; Czuba, E.; Monika, W.; Moryś, J.; Lietzau, G. Neurovascular unit as a source of ischemic stroke biomarkers-limitations of experimental studies and perspectives for clinical application. Transl. Stroke Res., 2020, 11(4), 553-579.
[http://dx.doi.org/10.1007/s12975-019-00744-5] [PMID: 31701356]
[18]
Hatashita, S.; Hoff, J.T. Brain edema and cerebrovascular permeability during cerebral ischemia in rats. Stroke, 1990, 21(4), 582-588.
[http://dx.doi.org/10.1161/01.STR.21.4.582] [PMID: 1691534]
[19]
Giraud, M.; Cho, T.H.; Nighoghossian, N.; Maucort-Boulch, D.; Deiana, G.; Østergaard, L.; Baron, J.C.; Fiehler, J.; Pedraza, S.; Derex, L.; Berthezène, Y. Early blood brain barrier changes in acute ischemic stroke: a sequential MRI study. J. Neuroimaging, 2015, 25(6), 959-963.
[http://dx.doi.org/10.1111/jon.12225] [PMID: 25702824]
[20]
Kuroiwa, T.; Ting, P.; Martinez, H.; Klatzo, I. The biphasic opening of the blood-brain barrier to proteins following temporary middle cerebral artery occlusion. Acta Neuropathol., 1985, 68(2), 122-129.
[http://dx.doi.org/10.1007/BF00688633] [PMID: 3907257]
[21]
Shi, Y.; Zhang, L.; Pu, H.; Mao, L.; Hu, X.; Jiang, X.; Xu, N.; Stetler, R.A.; Zhang, F.; Liu, X.; Leak, R.K.; Keep, R.F.; Ji, X.; Chen, J. Rapid endothelial cytoskeletal reorganization enables early blood-brain barrier disruption and long-term ischaemic reperfusion brain injury. Nat. Commun., 2016, 7, 10523.
[http://dx.doi.org/10.1038/ncomms10523] [PMID: 26813496]
[22]
Yang, Y.; Rosenberg, G.A. Blood-brain barrier breakdown in acute and chronic cerebrovascular disease. Stroke, 2011, 42(11), 3323-3328.
[http://dx.doi.org/10.1161/STROKEAHA.110.608257] [PMID: 21940972]
[23]
Engelhardt, B. Immune cell entry into the central nervous system: involvement of adhesion molecules and chemokines. J. Neurol. Sci., 2008, 274(1-2), 23-26.
[http://dx.doi.org/10.1016/j.jns.2008.05.019] [PMID: 18573502]
[24]
Liu, L.; Eckert, M.A.; Riazifar, H.; Kang, D.K.; Agalliu, D.; Zhao, W. From blood to the brain: can systemically transplanted mesenchymal stem cells cross the blood-brain barrier? Stem Cells Int., 2013, 2013, 435093.
[http://dx.doi.org/10.1155/2013/435093] [PMID: 23997771]
[25]
Sifat, A.E.; Vaidya, B.; Abbruscato, T.J. Blood-brain barrier protection as a therapeutic strategy for acute ischemic stroke. AAPS J., 2017, 19(4), 957-972.
[http://dx.doi.org/10.1208/s12248-017-0091-7] [PMID: 28484963]
[26]
Chen, H.; Guan, B.; Chen, X.; Chen, X.; Li, C.; Qiu, J.; Yang, D.; Liu, K.J.; Qi, S.; Shen, J. Baicalin attenuates blood-brain barrier disruption and hemorrhagic transformation and improves neurological outcome in ischemic stroke rats with delayed t-PA treatment: involvement of ONOO-MMP-9 pathway. Transl. Stroke Res., 2018, 9(5), 515-529.
[http://dx.doi.org/10.1007/s12975-017-0598-3] [PMID: 29275501]
[27]
Ayata, C.; Ropper, A.H. Ischaemic brain oedema. J. Clin. Neurosci., 2002, 9(2), 113-124.
[http://dx.doi.org/10.1054/jocn.2001.1031] [PMID: 11922696]
[28]
Lucivero, V.; Prontera, M.; Mezzapesa, D.M.; Petruzzellis, M.; Sancilio, M.; Tinelli, A.; Di Noia, D.; Ruggieri, M.; Federico, F. Different roles of matrix metalloproteinases-2 and -9 after human ischaemic stroke. Neurol. Sci., 2007, 28(4), 165-170.
[http://dx.doi.org/10.1007/s10072-007-0814-0] [PMID: 17690845]
[29]
Doetsch, F.; Caillé, I.; Lim, D.A.; García-Verdugo, J.M.; Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell, 1999, 97(6), 703-716.
[http://dx.doi.org/10.1016/S0092-8674(00)80783-7] [PMID: 10380923]
[30]
Djavadian, R.L. Serotonin and neurogenesis in the hippocampal dentate gyrus of adult mammals. Acta Neurobiol. Exp. (Warsz.), 2004, 64(2), 189-200.
[PMID: 15366252]
[31]
Kuhn, H.G.; Dickinson-Anson, H.; Gage, F.H. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J. Neurosci., 1996, 16(6), 2027-2033.
[http://dx.doi.org/10.1523/JNEUROSCI.16-06-02027.1996] [PMID: 8604047]
[32]
Jin, K.; Minami, M.; Lan, J.Q.; Mao, X.O.; Batteur, S.; Simon, R.P.; Greenberg, D.A. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc. Natl. Acad. Sci. USA, 2001, 98(8), 4710-4715.
[http://dx.doi.org/10.1073/pnas.081011098] [PMID: 11296300]
[33]
Ishibashi, S.; Sakaguchi, M.; Kuroiwa, T.; Yamasaki, M.; Kanemura, Y.; Shizuko, I.; Shimazaki, T.; Onodera, M.; Okano, H.; Mizusawa, H. Human neural stem/progenitor cells, expanded in long-term neurosphere culture, promote functional recovery after focal ischemia in Mongolian gerbils. J. Neurosci. Res., 2004, 78(2), 215-223.
[http://dx.doi.org/10.1002/jnr.20246] [PMID: 15378509]
[34]
Yagita, Y.; Kitagawa, K.; Ohtsuki, T. Takasawa Ki; Miyata, T.; Okano, H.; Hori, M.; Matsumoto, M. Neurogenesis by progenitor cells in the ischemic adult rat hippocampus. Stroke, 2001, 32(8), 1890-1896.
[http://dx.doi.org/10.1161/01.STR.32.8.1890] [PMID: 11486122]
[35]
Zhang, R.L.; Zhang, Z.G.; Zhang, L.; Chopp, M. Proliferation and differentiation of progenitor cells in the cortex and the subventricular zone in the adult rat after focal cerebral ischemia. Neuroscience, 2001, 105(1), 33-41.
[http://dx.doi.org/10.1016/S0306-4522(01)00117-8] [PMID: 11483298]
[36]
Tonchev, A.B.; Yamashima, T.; Sawamoto, K.; Okano, H. Enhanced proliferation of progenitor cells in the subventricular zone and limited neuronal production in the striatum and neocortex of adult macaque monkeys after global cerebral ischemia. J. Neurosci. Res., 2005, 81(6), 776-788.
[http://dx.doi.org/10.1002/jnr.20604] [PMID: 16047371]
[37]
Jin, K.; Wang, X.; Xie, L.; Mao, X.O.; Zhu, W.; Wang, Y.; Shen, J.; Mao, Y.; Banwait, S.; Greenberg, D.A. Evidence for stroke-induced neurogenesis in the human brain. Proc. Natl. Acad. Sci. USA, 2006, 103(35), 13198-13202.
[http://dx.doi.org/10.1073/pnas.0603512103] [PMID: 16924107]
[38]
Nakayama, D.; Matsuyama, T.; Ishibashi-Ueda, H.; Nakagomi, T.; Kasahara, Y.; Hirose, H.; Kikuchi-Taura, A.; Stern, D.M.; Mori, H.; Taguchi, A. Injury-induced neural stem/progenitor cells in post-stroke human cerebral cortex. Eur. J. Neurosci., 2010, 31(1), 90-98.
[http://dx.doi.org/10.1111/j.1460-9568.2009.07043.x] [PMID: 20104652]
[39]
Weissman, I.L.; Anderson, D.J.; Gage, F. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu. Rev. Cell Dev. Biol., 2001, 17, 387-403.
[http://dx.doi.org/10.1146/annurev.cellbio.17.1.387] [PMID: 11687494]
[40]
Hicks, C.; Stevanato, L.; Stroemer, R.P.; Tang, E.; Richardson, S.; Sinden, J.D. In vivo and in vitro characterization of the angiogenic effect of CTX0E03 human neural stem cells. Cell Transplant., 2013, 22(9), 1541-1552.
[http://dx.doi.org/10.3727/096368912X657936] [PMID: 23067568]
[41]
Banerjee, S.; Williamson, D.A.; Habib, N.; Chataway, J. The potential benefit of stem cell therapy after stroke: an update. Vasc. Health Risk Manag., 2012, 8, 569-580.
[http://dx.doi.org/10.2147/VHRM.S25745] [PMID: 23091389]
[42]
Li, L.; Chu, L.; Ren, C.; Wang, J.; Sun, S.; Li, T.; Yin, Y. Enhanced migration of bone marrow-derived mesenchymal stem cells with tetramethylpyrazine and its synergistic effect on angiogenesis and neurogenesis after cerebral ischemia in rats. Stem Cells Dev., 2019, 28(13), 871-881.
[http://dx.doi.org/10.1089/scd.2018.0254] [PMID: 31038013]
[43]
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]
[44]
Fischer, U.M.; Harting, M.T.; Jimenez, F.; Monzon-Posadas, W.O.; Xue, H.; Savitz, S.I.; Laine, G.A.; Cox, C.S., Jr Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect. Stem Cells Dev., 2009, 18(5), 683-692.
[http://dx.doi.org/10.1089/scd.2008.0253] [PMID: 19099374]
[45]
Ponte, A.L.; Marais, E.; Gallay, N.; Langonné, A.; Delorme, B.; Hérault, O.; Charbord, P.; Domenech, J. The in vitro migration capacity of human bone marrow mesenchymal stem cells: comparison of chemokine and growth factor chemotactic activities. Stem Cells, 2007, 25(7), 1737-1745.
[http://dx.doi.org/10.1634/stemcells.2007-0054] [PMID: 17395768]
[46]
Peled, A.; Kollet, O.; Ponomaryov, T.; Petit, I.; Franitza, S.; Grabovsky, V.; Slav, M.M.; Nagler, A.; Lider, O.; Alon, R.; Zipori, D.; Lapidot, T. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood, 2000, 95(11), 3289-3296.
[http://dx.doi.org/10.1182/blood.V95.11.3289] [PMID: 10828007]
[47]
Thomson, J.A.; Itskovitz-Eldor, J.; Shapiro, S.S.; Waknitz, M.A.; Swiergiel, J.J.; Marshall, V.S.; Jones, J.M. Embryonic stem cell lines derived from human blastocysts. Science, 1998, 282(5391), 1145-1147.
[http://dx.doi.org/10.1126/science.282.5391.1145] [PMID: 9804556]
[48]
Zhang, P.; Li, J.; Liu, Y.; Chen, X.; Kang, Q. Transplanted human embryonic neural stem cells survive, migrate, differentiate and increase endogenous nestin expression in adult rat cortical peri-infarction zone. Neuropathology, 2009, 29(4), 410-421.
[http://dx.doi.org/10.1111/j.1440-1789.2008.00993.x] [PMID: 19170896]
[49]
Nagai, N.; Kawao, N.; Okada, K.; Okumoto, K.; Teramura, T.; Ueshima, S.; Umemura, K.; Matsuo, O. Systemic transplantation of embryonic stem cells accelerates brain lesion decrease and angiogenesis. Neuroreport, 2010, 21(8), 575-579.
[http://dx.doi.org/10.1097/WNR.0b013e32833a7d2c] [PMID: 20431496]
[50]
Tae-Hoon, L.; Yoon-Seok, L. Transplantation of mouse embryonic stem cell after middle cerebral artery occlusion. Acta Cir. Bras., 2012, 27(4), 333-339.
[http://dx.doi.org/10.1590/S0102-86502012000400009] [PMID: 22534809]
[51]
Zimmermann, S.; Voss, M.; Kaiser, S.; Kapp, U.; Waller, C.F.; Martens, U.M. Lack of telomerase activity in human mesenchymal stem cells. Leukemia, 2003, 17(6), 1146-1149.
[http://dx.doi.org/10.1038/sj.leu.2402962] [PMID: 12764382]
[52]
Fisher, M. Pericyte signaling in the neurovascular unit. Stroke, 2009, 40(3)(Suppl.), S13-S15.
[http://dx.doi.org/10.1161/STROKEAHA.108.533117] [PMID: 19064799]
[53]
Honmou, O.; Onodera, R.; Sasaki, M.; Waxman, S.G.; Kocsis, J.D. Mesenchymal stem cells: therapeutic outlook for stroke. Trends Mol. Med., 2012, 18(5), 292-297.
[http://dx.doi.org/10.1016/j.molmed.2012.02.003] [PMID: 22459358]
[54]
Sundberg, C.; Kowanetz, M.; Brown, L.F.; Detmar, M.; Dvorak, H.F. Stable expression of angiopoietin-1 and other markers by cultured pericytes: phenotypic similarities to a subpopulation of cells in maturing vessels during later stages of angiogenesis in vivo. Lab. Invest., 2002, 82(4), 387-401.
[http://dx.doi.org/10.1038/labinvest.3780433] [PMID: 11950897]
[55]
Zhang, Z.G.; Zhang, L.; Croll, S.D.; Chopp, M. Angiopoietin-1 reduces cerebral blood vessel leakage and ischemic lesion volume after focal cerebral embolic ischemia in mice. Neuroscience, 2002, 113(3), 683-687.
[http://dx.doi.org/10.1016/S0306-4522(02)00175-6] [PMID: 12150788]
[56]
Tang, G.; Liu, Y.; Zhang, Z.; Lu, Y.; Wang, Y.; Huang, J.; Li, Y.; Chen, X.; Gu, X.; Wang, Y.; Yang, G.Y. Mesenchymal stem cells maintain blood-brain barrier integrity by inhibiting aquaporin-4 upregulation after cerebral ischemia. Stem Cells, 2014, 32(12), 3150-3162.
[http://dx.doi.org/10.1002/stem.1808] [PMID: 25100404]
[57]
Manley, G.T.; Fujimura, M.; Ma, T.; Noshita, N.; Filiz, F.; Bollen, A.W.; Chan, P.; Verkman, A.S. Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med., 2000, 6(2), 159-163.
[http://dx.doi.org/10.1038/72256] [PMID: 10655103]
[58]
Cheng, Z.; Wang, L.; Qu, M.; Liang, H.; Li, W.; Li, Y.; Deng, L.; Zhang, Z.; Yang, G.Y. Mesenchymal stem cells attenuate blood-brain barrier leakage after cerebral ischemia in mice. J. Neuroinflammation, 2018, 15(1), 135.
[http://dx.doi.org/10.1186/s12974-018-1153-1] [PMID: 29724240]
[59]
Namioka, T.; Namioka, A.; Sasaki, M.; Kataoka-Sasaki, Y.; Oka, S.; Nakazaki, M.; Onodera, R.; Suzuki, J.; Sasaki, Y.; Nagahama, H.; Kocsis, J.D.; Honmou, O. Intravenous infusion of mesenchymal stem cells promotes functional recovery in a rat model of chronic cerebral infarction. J. Neurosurg., 2018, 131, 1-8.
[PMID: 30485210]
[60]
Huang, Y.; Wang, J.; Cai, J.; Qiu, Y.; Zheng, H.; Lai, X.; Sui, X.; Wang, Y.; Lu, Q.; Zhang, Y.; Yuan, M.; Gong, J.; Cai, W.; Liu, X.; Shan, Y.; Deng, Z.; Shi, Y.; Shu, Y.; Zhang, L.; Qiu, W.; Peng, L.; Ren, J.; Lu, Z.; Xiang, A.P. Targeted homing of CCR2-overexpressing mesenchymal stromal cells to ischemic brain enhances post-stroke recovery partially through PRDX4-mediated blood-brain barrier preservation. Theranostics, 2018, 8(21), 5929-5944.
[http://dx.doi.org/10.7150/thno.28029] [PMID: 30613272]
[61]
Wei, Z.Z.; Gu, X.; Ferdinand, A.; Lee, J.H.; Ji, X.; Ji, X.M.; Yu, S.P.; Wei, L. Intranasal delivery of bone marrow mesenchymal stem cells improved neurovascular regeneration and rescued neuropsychiatric deficits after neonatal stroke in rats. Cell Transplant., 2015, 24(3), 391-402.
[http://dx.doi.org/10.3727/096368915X686887] [PMID: 25647744]
[62]
Nakazaki, M.; Sasaki, M.; Kataoka-Sasaki, Y.; Oka, S.; Suzuki, J.; Sasaki, Y.; Nagahama, H.; Hashi, K.; Kocsis, J.D.; Honmou, O. Intravenous infusion of mesenchymal stem cells improves impaired cognitive function in a cerebral small vessel disease model. Neuroscience, 2019, 408, 361-377.
[http://dx.doi.org/10.1016/j.neuroscience.2019.04.018] [PMID: 30999031]
[63]
Yoo, S.W.; Chang, D.Y.; Lee, H.S.; Kim, G.H.; Park, J.S.; Ryu, B.Y.; Joe, E.H.; Lee, Y.D.; Kim, S.S.; Suh-Kim, H. Immune following suppression mesenchymal stem cell transplantation in the ischemic brain is mediated by TGF-β. Neurobiol. Dis., 2013, 58, 249-257.
[http://dx.doi.org/10.1016/j.nbd.2013.06.001] [PMID: 23759293]
[64]
Che, X.; Ye, W.; Panga, L.; Wu, D.C.; Yang, G.Y. Monocyte chemoattractant protein-1 expressed in neurons and astrocytes during focal ischemia in mice. Brain Res., 2001, 902(2), 171-177.
[http://dx.doi.org/10.1016/S0006-8993(01)02328-9] [PMID: 11384610]
[65]
Strecker, J.K.; Minnerup, J.; Schütte-Nütgen, K.; Gess, B.; Schäbitz, W.R.; Schilling, M. Monocyte chemoattractant protein-1-deficiency results in altered blood-brain barrier breakdown after experimental stroke. Stroke, 2013, 44(9), 2536-2544.
[http://dx.doi.org/10.1161/STROKEAHA.111.000528] [PMID: 23821228]
[66]
Borlongan, C.V.; Hadman, M.; Sanberg, C.D.; Sanberg, P.R. Central nervous system entry of peripherally injected umbilical cord blood cells is not required for neuroprotection in stroke. Stroke, 2004, 35(10), 2385-2389.
[http://dx.doi.org/10.1161/01.STR.0000141680.49960.d7] [PMID: 15345799]
[67]
Huang, W.; Mo, X.; Qin, C.; Zheng, J.; Liang, Z.; Zhang, C. Transplantation of differentiated bone marrow stromal cells promotes motor functional recovery in rats with stroke. Neurol. Res., 2013, 35(3), 320-328.
[http://dx.doi.org/10.1179/1743132812Y.0000000151] [PMID: 23485057]
[68]
Leu, S.; Lin, Y.C.; Yuen, C.M.; Yen, C.H.; Kao, Y.H.; Sun, C.K.; Yip, H.K. Adipose-derived mesenchymal stem cells markedly attenuate brain infarct size and improve neurological function in rats. J. Transl. Med., 2010, 8, 63.
[http://dx.doi.org/10.1186/1479-5876-8-63] [PMID: 20584315]
[69]
Chi, L.; Huang, Y.; Mao, Y.; Wu, K.; Zhang, L.; Nan, G. Tail vein infusion of adipose-derived mesenchymal stem cell alleviated inflammatory response and improved blood brain barrier condition by suppressing endoplasmic reticulum stress in a middle cerebral artery occlusion rat model. Med. Sci. Monit., 2018, 24, 3946-3957.
[http://dx.doi.org/10.12659/MSM.907096] [PMID: 29888735]
[70]
Li, C.; Fei, K.; Tian, F.; Gao, C.; Yang, S. Adipose-derived mesenchymal stem cells attenuate ischemic brain injuries in rats by modulating miR-21-3p/MAT2B signaling transduction. Croat. Med. J., 2019, 60(5), 439-448.
[http://dx.doi.org/10.3325/cmj.2019.60.439] [PMID: 31686458]
[71]
Ge, X.; Li, W.; Huang, S.; Yin, Z.; Yang, M.; Han, Z.; Han, Z.; Chen, F.; Wang, H.; Lei, P.; Zhang, J. Increased miR-21-3p in Injured brain microvascular endothelial cells after traumatic brain injury aggravates blood-brain barrier damage by promoting cellular apoptosis and inflammation through targeting MAT2B. J. Neurotrauma, 2019, 36(8), 1291-1305.
[http://dx.doi.org/10.1089/neu.2018.5728] [PMID: 29695199]
[72]
Chen, J.; Sanberg, P.R.; Li, Y.; Wang, L.; Lu, M.; Willing, A.E.; Sanchez-Ramos, J.; Chopp, M. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke, 2001, 32(11), 2682-2688.
[http://dx.doi.org/10.1161/hs1101.098367] [PMID: 11692034]
[73]
Vendrame, M.; Cassady, J.; Newcomb, J.; Butler, T.; Pennypacker, K.R.; Zigova, T.; Sanberg, C.D.; Sanberg, P.R.; Willing, A.E. Infusion of human umbilical cord blood cells in a rat model of stroke dose-dependently rescues behavioral deficits and reduces infarct volume. Stroke, 2004, 35(10), 2390-2395.
[http://dx.doi.org/10.1161/01.STR.0000141681.06735.9b] [PMID: 15322304]
[74]
Lind, J.; Cheng, C.; Hadman, M.; Goodman, D.; Chopp, M.; Borlongan, C.V. Transplanted stroke animals display normalized cerebral blood flow and BBB permeability during onset of behavioral recovery. IBNS; , 2003.
[75]
Zhao, Q.; Hu, J.; Xiang, J.; Gu, Y.; Jin, P.; Hua, F.; Zhang, Z.; Liu, Y.; Zan, K.; Zhang, Z.; Zu, J.; Yang, X.; Shi, H.; Zhu, J.; Xu, Y.; Cui, G.; Ye, X. Intranasal administration of human umbilical cord mesenchymal stem cells-conditioned medium enhances vascular remodeling after stroke. Brain Res., 2015, 1624, 489-496.
[http://dx.doi.org/10.1016/j.brainres.2015.08.003] [PMID: 26279113]
[76]
Cui, X.; Chopp, M.; Zacharek, A.; Ye, X.; Roberts, C.; Chen, J. Angiopoietin/Tie2 pathway mediates type 2 diabetes induced vascular damage after cerebral stroke. Neurobiol. Dis., 2011, 43(1), 285-292.
[http://dx.doi.org/10.1016/j.nbd.2011.04.005] [PMID: 21515377]
[77]
Cui, X.; Chopp, M.; Zacharek, A.; Dai, J.; Zhang, C.; Yan, T.; Ning, R.; Roberts, C.; Shehadah, A.; Kuzmin-Nichols, N.; Sanberg, C.D.; Chen, J. Combination treatment of stroke with sub-therapeutic doses of Simvastatin and human umbilical cord blood cells enhances vascular remodeling and improves functional outcome. Neuroscience, 2012, 227, 223-231.
[http://dx.doi.org/10.1016/j.neuroscience.2012.09.066] [PMID: 23041512]
[78]
Shiao, M.L.; Yuan, C.; Crane, A.T.; Voth, J.P.; Juliano, M.; Stone, L.L.H.; Nan, Z.; Zhang, Y.; Kuzmin-Nichols, N.; Sanberg, P.R.; Grande, A.W.; Low, W.C. Immunomodulation with human umbilical cord blood stem cells ameliorates ischemic brain injury - a brain transcriptome profiling analysis. Cell Transplant., 2019, 28(7), 864-873.
[http://dx.doi.org/10.1177/0963689719836763] [PMID: 31066288]
[79]
Kholodenko, I.V.; Yarygin, K.N.; Gubsky, L.V.; Konieva, A.A.; Tairova, R.T.; Povarova, O.V.; Kholodenko, R.V.; Burunova, V.V.; Yarygin, V.N.; Skvortsova, V.I. Intravenous xenotransplantation of human placental mesenchymal stem cells to rats: comparative analysis of homing in rat brain in two models of experimental ischemic stroke. Bull. Exp. Biol. Med., 2012, 154(1), 118-123.
[http://dx.doi.org/10.1007/s10517-012-1890-6] [PMID: 23330106]
[80]
Faezi, M.; Nasseri Maleki, S.; Aboutaleb, N.; Nikougoftar, M. The membrane mesenchymal stem cell derived conditioned medium exerts neuroprotection against focal cerebral ischemia by targeting apoptosis. J. Chem. Neuroanat., 2018, 94, 21-31.
[http://dx.doi.org/10.1016/j.jchemneu.2018.08.004] [PMID: 30121327]
[81]
Nazarinia, D.; Aboutaleb, N.; Gholamzadeh, R.; Nasseri Maleki, S.; Mokhtari, B.; Nikougoftar, M. Conditioned medium obtained from human amniotic mesenchymal stem cells attenuates focal cerebral ischemia/reperfusion injury in rats by targeting mTOR pathway. J. Chem. Neuroanat., 2019, 102, 101707.
[http://dx.doi.org/10.1016/j.jchemneu.2019.101707] [PMID: 31672459]
[82]
Lin, R.; Cai, J.; Nathan, C.; Wei, X.; Schleidt, S.; Rosenwasser, R.; Iacovitti, L. Neurogenesis is enhanced by stroke in multiple new stem cell niches along the ventricular system at sites of high BBB permeability. Neurobiol. Dis., 2015, 74, 229-239.
[http://dx.doi.org/10.1016/j.nbd.2014.11.016] [PMID: 25484283]
[83]
Darsalia, V.; Kallur, T.; Kokaia, Z. Survival, migration and neuronal differentiation of human fetal striatal and cortical neural stem cells grafted in stroke-damaged rat striatum. Eur. J. Neurosci., 2007, 26(3), 605-614.
[http://dx.doi.org/10.1111/j.1460-9568.2007.05702.x] [PMID: 17686040]
[84]
Guzman, R.; Bliss, T.; De Los Angeles, A.; Moseley, M.; Palmer, T.; Steinberg, G. Neural progenitor cells transplanted into the uninjured brain undergo targeted migration after stroke onset. J. Neurosci. Res., 2008, 86(4), 873-882.
[http://dx.doi.org/10.1002/jnr.21542] [PMID: 17975825]
[85]
Huang, L.; Wong, S.; Snyder, E.Y.; Hamblin, M.H.; Lee, J.P. Human neural stem cells rapidly ameliorate symptomatic inflammation in early-stage ischemic-reperfusion cerebral injury. Stem Cell Res. Ther., 2014, 5(6), 129.
[http://dx.doi.org/10.1186/scrt519] [PMID: 25418536]
[86]
Eckert, A.; Huang, L.; Gonzalez, R.; Kim, H.S.; Hamblin, M.H.; Lee, J.P. Bystander effect fuels human induced pluripotent stem cell-derived neural stem cells to quickly attenuate early stage neurological deficits after stroke. Stem Cells Transl. Med., 2015, 4(7), 841-851.
[http://dx.doi.org/10.5966/sctm.2014-0184] [PMID: 26025980]
[87]
Zhang, T.; Yang, X.; Liu, T.; Shao, J.; Fu, N.; Yan, A.; Geng, K.; Xia, W. Adjudin-preconditioned neural stem cells enhance neuroprotection after ischemia reperfusion in mice. Stem Cell Res. Ther., 2017, 8(1), 248.
[http://dx.doi.org/10.1186/s13287-017-0677-0] [PMID: 29115993]
[88]
Liu, T.; Zhang, T.; Yu, H.; Shen, H.; Xia, W. Adjudin protects against cerebral ischemia reperfusion injury by inhibition of neuroinflammation and blood-brain barrier disruption. J. Neuroinflammation, 2014, 11, 107.
[http://dx.doi.org/10.1186/1742-2094-11-107] [PMID: 24927761]
[89]
Doeppner, T.R.; Ewert, T.A.; Tönges, L.; Herz, J.; Zechariah, A.; ElAli, A.; Ludwig, A.K.; Giebel, B.; Nagel, F.; Dietz, G.P.; 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]
[90]
Doeppner, T.R.; Kaltwasser, B.; Teli, M.K.; Sanchez-Mendoza, E.H.; Kilic, E.; Bähr, M.; Hermann, D.M. Post-stroke transplantation of adult subventricular zone derived neural progenitor cells--A comprehensive analysis of cell delivery routes and their underlying mechanisms. Exp. Neurol., 2015, 273, 45-56.
[http://dx.doi.org/10.1016/j.expneurol.2015.07.023] [PMID: 26253224]
[91]
Doeppner, T.R.; Kaltwasser, B.; Teli, M.K.; Bretschneider, E.; Bähr, M.; Hermann, D.M. Effects of acute versus post-acute systemic delivery of neural progenitor cells on neurological recovery and brain remodeling after focal cerebral ischemia in mice. Cell Death Dis., 2014, 5(8), e1386.
[http://dx.doi.org/10.1038/cddis.2014.359] [PMID: 25144721]
[92]
Hristov, M.; Erl, W.; Weber, P.C. Endothelial progenitor cells: mobilization, differentiation, and homing. Arterioscler. Thromb. Vasc. Biol., 2003, 23(7), 1185-1189.
[http://dx.doi.org/10.1161/01.ATV.0000073832.49290.B5] [PMID: 12714439]
[93]
Yip, H.K.; Chang, L.T.; Chang, W.N.; Lu, C.H.; Liou, C.W.; Lan, M.Y.; Liu, J.S.; Youssef, A.A.; Chang, H.W. Level and value of circulating endothelial progenitor cells in patients after acute ischemic stroke. Stroke, 2008, 39(1), 69-74.
[http://dx.doi.org/10.1161/STROKEAHA.107.489401] [PMID: 18063830]
[94]
Fan, Y.; Shen, F.; Frenzel, T.; Zhu, W.; Ye, J.; Liu, J.; Chen, Y.; Su, H.; Young, W.L.; Yang, G.Y. Endothelial progenitor cell transplantation improves long-term stroke outcome in mice. Ann. Neurol., 2010, 67(4), 488-497.
[http://dx.doi.org/10.1002/ana.21919] [PMID: 20437584]
[95]
Iskander, A.; Knight, R.A.; Zhang, Z.G.; Ewing, J.R.; Shankar, A.; Varma, N.R.; Bagher-Ebadian, H.; Ali, M.M.; Arbab, A.S.; Janic, B. Intravenous administration of human umbilical cord blood-derived AC133+ endothelial progenitor cells in rat stroke model reduces infarct volume: magnetic resonance imaging and histological findings. Stem Cells Transl. Med., 2013, 2(9), 703-714.
[http://dx.doi.org/10.5966/sctm.2013-0066] [PMID: 23934909]
[96]
Garbuzova-Davis, S.; Haller, E.; Lin, R.; Borlongan, C.V. Intravenously transplanted human bone marrow endothelial progenitor cells engraft within brain capillaries, preserve mitochondrial morphology, and display pinocytotic activity toward blood-brain barrier repair in ischemic stroke rats. Stem Cells, 2017, 35(5), 1246-1258.
[http://dx.doi.org/10.1002/stem.2578] [PMID: 28142208]
[97]
Ding, J.; Zhang, Y.; Wang, C.X.; Li, P.C.; Zhao, Z.; Wang, C.; Teng, G.J. Dual-modality imaging of endothelial progenitor cells transplanted after ischaemic photothrombotic stroke. Life Sci., 2019, 239, 116774.
[http://dx.doi.org/10.1016/j.lfs.2019.116774] [PMID: 31689438]
[98]
Sargento-Freitas, J.; Aday, S.; Nunes, C.; Cordeiro, M.; Gouveia, A.; Silva, F.; Machado, C.; Rodrigues, B.; Santo, G.C.; Ferreira, C.; Amorim, A.; Sousa, S.; Gomes, A.C.; Castelo-Branco, M.; Ferreira, L.; Cunha, L. Endothelial progenitor cells enhance blood-brain barrier permeability in subacute stroke. Neurology, 2018, 90(2), e127-e134.
[http://dx.doi.org/10.1212/WNL.0000000000004801] [PMID: 29237797]
[99]
Leong, W.K.; Henshall, T.L.; Arthur, A.; Kremer, K.L.; Lewis, M.D.; Helps, S.C.; Field, J.; Hamilton-Bruce, M.A.; Warming, S.; Manavis, J.; Vink, R.; Gronthos, S.; Koblar, S.A. Human adult dental pulp stem cells enhance poststroke functional recovery through non-neural replacement mechanisms. Stem Cells Transl. Med., 2012, 1(3), 177-187.
[http://dx.doi.org/10.5966/sctm.2011-0039] [PMID: 23197777]
[100]
Borlongan, C.V.; Kaneko, Y.; Maki, M.; Yu, S.J.; Ali, M.; Allickson, J.G.; Sanberg, C.D.; Kuzmin-Nichols, N.; Sanberg, P.R. Menstrual blood cells display stem cell-like phenotypic markers and exert neuroprotection following transplantation in experimental stroke. Stem Cells Dev., 2010, 19(4), 439-452.
[http://dx.doi.org/10.1089/scd.2009.0340] [PMID: 19860544]
[101]
Hassiotou, F.; Beltran, A.; Chetwynd, E.; Stuebe, A.M.; Twigger, A.J.; Metzger, P.; Trengove, N.; Lai, C.T.; Filgueira, L.; Blancafort, P.; Hartmann, P.E. Breastmilk is a novel source of stem cells with multilineage differentiation potential. Stem Cells, 2012, 30(10), 2164-2174.
[http://dx.doi.org/10.1002/stem.1188] [PMID: 22865647]
[102]
Sowa, K.; Nito, C.; Nakajima, M.; Suda, S.; Nishiyama, Y.; Sakamoto, Y.; Nitahara-Kasahara, Y.; Nakamura-Takahashi, A.; Ueda, M.; Kimura, K.; Okada, T. Impact of dental pulp stem cells overexpressing hepatocyte growth factor after cerebral ischemia/reperfusion in rats. Mol. Ther. Methods Clin. Dev., 2018, 10, 281-290.
[http://dx.doi.org/10.1016/j.omtm.2018.07.009] [PMID: 30151417]
[103]
Bosche, B.; Mergenthaler, P.; Doeppner, T.R.; Hescheler, J.; Molcanyi, M. Complex clearance mechanisms after intraventricular hemorrhage and rt-PA treatment-a review on clinical trials. Transl. Stroke Res., 2020, 11(3), 337-344.
[http://dx.doi.org/10.1007/s12975-019-00735-6] [PMID: 31522408]
[104]
Nakazaki, M.; Sasaki, M.; Kataoka-Sasaki, Y.; Oka, S.; Namioka, T.; Namioka, A.; Onodera, R.; Suzuki, J.; Sasaki, Y.; Nagahama, H.; Mikami, T.; Wanibuchi, M.; Kocsis, J.D.; Honmou, O. Intravenous infusion of mesenchymal stem cells inhibits intracranial hemorrhage after recombinant tissue plasminogen activator therapy for transient middle cerebral artery occlusion in rats. J. Neurosurg., 2017, 127(4), 917-926.
[http://dx.doi.org/10.3171/2016.8.JNS16240] [PMID: 28059661]
[105]
Yang, B.; Li, W.; Satani, N.; Nghiem, D.M.; Xi, X.; Aronowski, J.; Savitz, S.I. Protective effects of autologous bone marrow mononuclear cells after administering t-PA in an embolic stroke model. Transl. Stroke Res., 2018, 9(2), 135-145.
[http://dx.doi.org/10.1007/s12975-017-0563-1] [PMID: 28836238]
[106]
Liu, N.; Deguchi, K.; Yamashita, T.; Liu, W.; Ikeda, Y.; Abe, K. Intracerebral transplantation of bone marrow stromal cells ameliorates tissue plasminogen activator-induced brain damage after cerebral ischemia in mice detected by in vivo and ex vivo optical imag.
[http://dx.doi.org/10.1002/jnr.23104] [PMID: 22791305]
[107]
Boese, A.C.; Eckert, A.; Hamblin, M.H.; Lee, J.P. Human neural stem cells improve early stage stroke outcome in delayed tissue plasminogen activator-treated aged stroke brains. Exp. Neurol., 2020, 329, 113275.
[http://dx.doi.org/10.1016/j.expneurol.2020.113275] [PMID: 32147438]
[108]
Chen, J.; Cui, X.; Zacharek, A.; Cui, Y.; Roberts, C.; Chopp, M. White matter damage and the effect of matrix metalloproteinases in type 2 diabetic mice after stroke. Stroke, 2011, 42(2), 445-452.
[http://dx.doi.org/10.1161/STROKEAHA.110.596486] [PMID: 21193743]
[109]
Chen, J.; Ye, X.; Yan, T.; Zhang, C.; Yang, X.P.; Cui, X.; Cui, Y.; Zacharek, A.; Roberts, C.; Liu, X.; Dai, X.; Lu, M.; Chopp, M. Adverse effects of bone marrow stromal cell treatment of stroke in diabetic rats. Stroke, 2011, 42(12), 3551-3558.
[http://dx.doi.org/10.1161/STROKEAHA.111.627174] [PMID: 21940967]
[110]
Yan, T.; Ye, X.; Chopp, M.; Zacharek, A.; Ning, R.; Venkat, P.; Roberts, C.; Lu, M.; Chen, J. Niaspan attenuates the adverse effects of bone marrow stromal cell treatment of stroke in type one diabetic rats. PLoS One, 2013, 8(11), e81199.
[http://dx.doi.org/10.1371/journal.pone.0081199] [PMID: 24303036]
[111]
Hu, J.; Liu, B.; Zhao, Q.; Jin, P.; Hua, F.; Zhang, Z.; Liu, Y.; Zan, K.; Cui, G.; Ye, X. Bone marrow stromal cells inhibits HMGB1-mediated inflammation after stroke in type 2 diabetic rats. Neuroscience, 2016, 324, 11-19.
[http://dx.doi.org/10.1016/j.neuroscience.2016.02.058] [PMID: 26946264]
[112]
Kim, J.B.; Sig Choi, J.; Yu, Y.M.; Nam, K.; Piao, C.S.; Kim, S.W.; Lee, M.H.; Han, P.L.; Park, J.S.; Lee, J.K. HMGB1, a novel cytokine-like mediator linking acute neuronal death and delayed neuroinflammation in the postischemic brain. J. Neurosci., 2006, 26(24), 6413-6421.
[http://dx.doi.org/10.1523/JNEUROSCI.3815-05.2006] [PMID: 16775128]
[113]
Zhang, J.; Takahashi, H.K.; Liu, K.; Wake, H.; Liu, R.; Maruo, T.; Date, I.; Yoshino, T.; Ohtsuka, A.; Mori, S.; Nishibori, M. Anti-high mobility group box-1 monoclonal antibody protects the blood-brain barrier from ischemia-induced disruption in rats. Stroke, 2011, 42(5), 1420-1428.
[http://dx.doi.org/10.1161/STROKEAHA.110.598334] [PMID: 21474801]
[114]
Xiang, J.; Hu, J.; Shen, T.; Liu, B.; Hua, F.; Zan, K.; Zu, J.; Cui, G.; Ye, X. Bone marrow mesenchymal stem cells-conditioned medium enhances vascular remodeling after stroke in type 2 diabetic rats. Neurosci. Lett., 2017, 644, 62-66.
[http://dx.doi.org/10.1016/j.neulet.2017.02.040] [PMID: 28219791]
[115]
Yan, T.; Venkat, P.; Chopp, M.; Zacharek, A.; Ning, R.; Roberts, C.; Zhang, Y.; Lu, M.; Chen, J. Neurorestorative responses to delayed human mesenchymal stromal cells treatment of stroke in type 2 diabetic rats. Stroke, 2016, 47(11), 2850-2858.
[http://dx.doi.org/10.1161/STROKEAHA.116.014686] [PMID: 27729575]
[116]
Ding, G.; Chen, J.; Chopp, M.; Li, L.; Yan, T.; Li, Q.; Cui, C.; Davarani, S.P.; Jiang, Q. Cell treatment for stroke in type two diabetic rats improves vascular permeability measured by MRI. PLoS One, 2016, 11(2), e0149147.
[http://dx.doi.org/10.1371/journal.pone.0149147] [PMID: 26900843]
[117]
Yan, T.; Venkat, P.; Ye, X.; Chopp, M.; Zacharek, A.; Ning, R.; Cui, Y.; Roberts, C.; Kuzmin-Nichols, N.; Sanberg, C.D.; Chen, J. HUCBCs increase angiopoietin 1 and induce neurorestorative effects after stroke in T1DM rats. CNS Neurosci. Ther., 2014, 20(10), 935-944.
[http://dx.doi.org/10.1111/cns.12307] [PMID: 25042092]
[118]
Chen, J.; Ning, R.; Zacharek, A.; Cui, C.; Cui, X.; Yan, T.; Venkat, P.; Zhang, Y.; Chopp, M. MiR-126 contributes to human umbilical cord blood cell-induced neurorestorative effects after stroke in type-2 diabetic mice. Stem Cells, 2016, 34(1), 102-113.
[http://dx.doi.org/10.1002/stem.2193] [PMID: 26299579]
[119]
Yan, T.; Venkat, P.; Chopp, M.; Zacharek, A.; Ning, R.; Cui, Y.; Roberts, C.; Kuzmin-Nichols, N.; Sanberg, C.D.; Chen, J. Neurorestorative therapy of stroke in type 2 diabetes mellitus rats treated with human umbilical cord blood cells. Stroke, 2015, 46(9), 2599-2606.
[http://dx.doi.org/10.1161/STROKEAHA.115.009870] [PMID: 26243222]
[120]
Geng, J.; Wang, L.; Qu, M.; Song, Y.; Lin, X.; Chen, Y.; Mamtilahun, M.; Chen, S.; Zhang, Z.; Wang, Y.; Yang, G.Y. Endothelial progenitor cells transplantation attenuated blood-brain barrier damage after ischemia in diabetic mice via HIF-1α. Stem Cell Res. Ther., 2017, 8(1), 163.
[http://dx.doi.org/10.1186/s13287-017-0605-3] [PMID: 28697748]
[121]
Semenza, G.L. Hypoxia-inducible factors in physiology and medicine. Cell, 2012, 148(3), 399-408.
[http://dx.doi.org/10.1016/j.cell.2012.01.021] [PMID: 22304911]
[122]
Boncoraglio, G.B.; Bersano, A.; Candelise, L.; Reynolds, B.A.; Parati, E.A. Stem cell transplantation for ischemic stroke. Cochrance. Database. Syst. Rev, 2010, 9, CD007231.
[123]
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]
[124]
Chang, Y.S.; Ahn, S.Y.; Yoo, H.S.; Sung, S.I.; Choi, S.J.; Oh, W.I.; Park, W.S. Mesenchymal stem cells for bronchopulmonary dysplasia: phase 1 dose-escalation clinical trial. J. Pediatr., 2014, 164(5), 966-972.e6.
[http://dx.doi.org/10.1016/j.jpeds.2013.12.011] [PMID: 24508444]

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