Research progress of different types of stem cells in treatment of ischemic stroke_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

CHEN Qiuzhu , LI Ling ,  XIE Huiqi

Laboratory of Stem Cell and Tissue Engineering, West China Hospital, Sichuan University, Chengdu Sichuan, 610041, P.R.China;

Corresponding author：

XIE Huiqi, Email: xiehuiqi@163.com

Keywords：

Stem cells; ischemic stroke; transplantation; stem cell therapy

DOI：

10.7507/1002-1892.202004160

Video：

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Objective To review the recent research progress of different types of stem cells in the treatment of ischemic stroke.Methods By searching the PubMed database, a systematic review had been carried out for the results of applying different types of stem cells in the treatment of ischemic stroke between 2000 and 2020.Results Stem cells can be transplanted via intracranial, intravascular, cerebrospinal fluid, and intranasal route in the treatment of ischemic stroke. Paracrine and cell replacement are the two major mechanisms of the therapy. The researches have mainly focused on utilization of neural stem cells, embryonic stem cells, and mesenchymal stem cells. Each has its own advantages and disadvantages in terms of capability of migration, survival rate, and safety. Certain stem cell therapies have completed phase one clinical trial.Conclusion Stem cells transplantation is feasible and has a great potential for the treatment of ischemic stroke, albeit that certain obstacles, including the selection of stem cells, transplantation strategy, migration ability, survival rate, still wait to be solved.

Citation： CHEN Qiuzhu, LI Ling, XIE Huiqi. Research progress of different types of stem cells in treatment of ischemic stroke. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(1): 111-117. doi: 10.7507/1002-1892.202004160 Copy

1.	Neuhaus AA, Couch Y, Hadley G, et al. Neuroprotection in stroke: the importance of collaboration and reproducibility. Brain, 2017, 140(8): 2079-2092.
2.	Song S, Liang L, Fonarow GC, et al. Comparison of clinical care and in-hospital outcomes of Asian American and White Patients with acute ischemic stroke. JAMA Neurol, 2019, 76(4): 430-439.
3.	Doeppner TR, Bähr M, Hermann DM, et al. Concise review: extracellular vesicles overcoming limitations of cell therapies in ischemic stroke. Stem Cells Transl Med, 2017, 6(11): 2044-2052.
4.	Wardlaw JM, Murray V, Berge E, et al. Thrombolysis for acute ischaemic stroke. Cochrane Database Syst Rev, 2014, 7(4): Cd000213.
5.	Liu X, Ye R, Yan T, et al. Cell based therapies for ischemic stroke: from basic science to bedside. Prog Neurobiol, 2014, 115: 92-115.
6.	Bernstock JD, Peruzzotti-Jametti L, Ye D, et al. Neural stem cell transplantation in ischemic stroke: A role for preconditioning and cellular engineering. J Cereb Blood Flow Metab, 2017, 37(7): 2314-2319.
7.	Zhang J, Chopp M. Cell-based therapy for ischemic stroke. Expert Opin Biol Ther, 2013, 13(9): 1229-1240.
8.	Horie N, Pereira MP, Niizuma K, et al. Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells, 2011, 29(2): 274-285.
9.	Andres RH, Horie N, Slikker W, et al. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain, 2011, 134(Pt 6): 1777-1789.
10.	Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature, 2005, 436(7048): 193-200.
11.	Imitola J, Raddassi K, Park KI, et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A, 2004, 101(52): 18117-18122.
12.	Yan YP, Sailor KA, Lang BT, et al. Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J Cereb Blood Flow Metab, 2007, 27(6): 1213-1224.
13.	Horie N, Hiu T, Nagata I. Stem cell transplantation enhances endogenous brain repair after experimental stroke. Neurol Med Chir (Tokyo), 2015, 55(2): 107-112.
14.	Sinden JD, Hicks C, Stroemer P, et al. Human neural stem cell therapy for chronic ischemic stroke: charting progress from laboratory to patients. Stem Cells Dev, 2017, 26(13): 933-947.
15.	Aday S, Zoldan J, Besnier M, et al. Synthetic microparticles conjugated with VEGF₁₆₅ improve the survival of endothelial progenitor cells via microRNA-17 inhibition. Nat Commun, 2017, 8(1): 747.
16.	Stonesifer C, Corey S, Ghanekar S, et al. Stem cell therapy for abrogating stroke-induced neuroinflammation and relevant secondary cell death mechanisms. Prog Neurobiol, 2017, 158: 94-131.
17.	Loubinoux I, Demain B, Davoust C, et al. Stem cells and motor recovery after stroke. Ann Phys Rehabil Med, 2014, 57(8): 499-508.
18.	Yamashita T, Liu W, Matsumura Y, et al. Novel therapeutic transplantation of induced neural stem cells for stroke. Cell Transplant, 2017, 26(3): 461-467.
19.	Kubis N. Stroke and the cell therapy saga: towards a safe, swift and efficient utilization of cells. Keio J Med, 2017, 66(3): 55.
20.	Tanaka E, Ogawa Y, Mukai T, et al. Dose-dependent effect of intravenous administration of human umbilical cord-derived mesenchymal stem cells in neonatal stroke mice. Front Neurol, 2018, 9: 133.
21.	Lazarov O, Mattson MP, Peterson DA, et al. When neurogenesis encounters aging and disease. Trends Neurosci, 2010, 33(12): 569-579.
22.	Wang F, Tang H, Zhu J, et al. Transplanting mesenchymal stem cells for treatment of ischemic stroke. Cell Transplant, 2018, 27(12): 1825-1834.
23.	Huang L, Zhang L. Neural stem cell therapies and hypoxic-ischemic brain injury. Prog Neurobiol, 2019, 173: 1-17.
24.	Jiang XC, Xiang JJ, Wu HH, et al. Neural stem cells transfected with reactive oxygen species-responsive polyplexes for effective treatment of ischemic stroke. Adv Mater, 2019, 31(10): e1807591.
25.	Jiang Y, Wei N, Zhu J, et al. Effects of brain-derived neurotrophic factor on local inflammation in experimental stroke of rat. Mediators Inflamm, 2010, 2010: 372423.
26.	Lee HJ, Lim IJ, Lee MC, et al. 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.
27.	Hass R, Kasper C, Böhm S, et al. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal, 2011, 9(1): 12.
28.	Huang P, Gebhart N, Richelson E, et al. Mechanism of mesenchymal stem cell-induced neuron recovery and anti-inflammation. Cytotherapy, 2014, 16(10): 1336-1344.
29.	Gu N, Rao C, Tian Y, et al. Anti-inflammatory and antiapoptotic effects of mesenchymal stem cells transplantation in rat brain with cerebral ischemia. J Stroke Cerebrovasc Dis, 2014, 23(10): 2598-2606.
30.	Wei L, Fraser JL, Lu ZY, et al. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis, 2012, 46(3): 635-645.
31.	Liu K, Guo L, Zhou Z, et al. Mesenchymal stem cells transfer mitochondria into cerebral microvasculature and promote recovery from ischemic stroke. Microvasc Res, 2019, 123: 74-80.
32.	Hayakawa K, Esposito E, Wang X, et al. Transfer of mitochondria from astrocytes to neurons after stroke. Nature, 2016, 535(7613): 551-555.
33.	Sheikh AM, Yano S, Mitaki S, et al. A Mesenchymal stem cell line (B10) increases angiogenesis in a rat MCAO model. Exp Neurol, 2019, 311: 182-193.
34.	Cheng Z, Wang L, Qu M, et al. Mesenchymal stem cells attenuate blood-brain barrier leakage after cerebral ischemia in mice. J Neuroinflammation, 2018, 15(1): 135.
35.	Bühnemann C, Scholz A, Bernreuther C, et al. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain, 2006, 129(Pt 12): 3238-3248.
36.	Wei L, Cui L, Snider BJ, et al. Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis, 2005, 19(1-2): 183-193.
37.	Drury-Stewart D, Song M, Mohamad O, et al. Highly efficient differentiation of neural precursors from human embryonic stem cells and benefits of transplantation after ischemic stroke in mice. Stem Cell Res Ther, 2013, 4(4): 93.
38.	Kosi N, Alić I, Salamon I, et al. Stroke promotes survival of nearby transplanted neural stem cells by decreasing their activation of caspase 3 while not affecting their differentiation. Neurosci Lett, 2018, 666: 111-119.
39.	Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron, 2008, 57(2): 178-201.
40.	Abbott NJ, Patabendige AA, Dolman DE, et al. Structure and function of the blood-brain barrier. Neurobiol Dis, 2010, 37(1): 13-25.
41.	Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol, 2015, 7(1): a020412.
42.	Stamatovic SM, Keep RF, Andjelkovic AV. Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr Neuropharmacol, 2008, 6(3): 179-192.
43.	Pendharkar AV, Chua JY, Andres RH, et al. Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke, 2010, 41(9): 2064-2070.
44.	Hersh DS, Wadajkar AS, Roberts N, et al. Evolving drug delivery strategies to overcome the blood brain barrier. Curr Pharm Des, 2016, 22(9): 1177-1193.
45.	Jin K, Sun Y, Xie L, et al. Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol Dis, 2005, 18(2): 366-374.
46.	Sharp J, Keirstead HS. Stem cell-based cell replacement strategies for the central nervous system. Neurosci Lett, 2009, 456(3): 107-111.
47.	Jiang Y, Zhu J, Xu G, et al. Intranasal delivery of stem cells to the brain. Expert Opin Drug Deliv, 2011, 8(5): 623-632.
48.	Danielyan L, Schäfer R, von Ameln-Mayerhofer A, et al. Intranasal delivery of cells to the brain. Eur J Cell Biol, 2009, 88(6): 315-324.
49.	Wilson EH, Weninger W, Hunter CA. Trafficking of immune cells in the central nervous system. J Clin Invest, 2010, 120(5): 1368-1379.
50.	Liu L, Eckert MA, Riazifar H, et al. From blood to the brain: can systemically transplanted mesenchymal stem cells cross the blood-brain barrier? Stem Cells Int, 2013, 2013: 435093.
51.	Teo GS, Ankrum JA, Martinelli R, et al. Mesenchymal stem cells transmigrate between and directly through tumor necrosis factor-α-activated endothelial cells via both leukocyte-like and novel mechanisms. Stem Cells, 2012, 30(11): 2472-2486.
52.	Steingen C, Brenig F, Baumgartner L, et al. Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J Mol Cell Cardiol, 2008, 44(6): 1072-1084.
53.	Yilmaz G, Vital S, Yilmaz CE, et al. Selectin-mediated recruitment of bone marrow stromal cells in the postischemic cerebral microvasculature. Stroke, 2011, 42(3): 806-811.
54.	Conaty P, Sherman LS, Naaldijk Y, et al. Methods of mesenchymal stem cell homing to the blood-brain barrier. Methods Mol Biol, 2018, 1842: 81-91.
55.	Freeman WD. Management of intracranial pressure. Continuum (Minneap Minn), 2015, 21(5 Neurocritical Care): 1299-1323.
56.	Gonzales-Portillo GS, Sanberg PR, Franzblau M, et al. Mannitol-enhanced delivery of stem cells and their growth factors across the blood-brain barrier. Cell Transplant, 2014, 23(4-5): 531-539.
57.	Seyfried DM, Han Y, Yang D, et al. Mannitol enhances delivery of marrow stromal cells to the brain after experimental intracerebral hemorrhage. Brain Res, 2008, 1224: 12-19.
58.	Shen WB, Anastasiadis P, Nguyen B, et al. Magnetic enhancement of stem cell-targeted delivery into the brain following MR-guided focused ultrasound for opening the blood-brain barrier. Cell Transplant, 2017, 26(7): 1235-1246.
59.	Burgess A, Ayala-Grosso CA, Ganguly M, et al. Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS One, 2011, 6(11): e27877.
60.	Wolburg H, Wolburg-Buchholz K, Engelhardt B. Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves tight junctions intact. Acta Neuropathol, 2005, 109(2): 181-190.
61.	Prasad K, Sharma A, Garg A, et al. Intravenous autologous bone marrow mononuclear stem cell therapy for ischemic stroke: a multicentric, randomized trial. Stroke, 2014, 45(12): 3618-3624.
62.	Banerjee S, Bentley P, Hamady M, et al. Intra-arterial immunoselected CD34+ stem cells for acute ischemic stroke. Stem Cells Transl Med, 2014, 3(11): 1322-1330.
63.	Díez-Tejedor E, Gutiérrez-Fernández M, Martínez-Sánchez P, et al. 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.
64.	Steinberg GK, Kondziolka D, Wechsler LR, et al. Two-year safety and clinical outcomes in chronic ischemic stroke patients after implantation of modified bone marrow-derived mesenchymal stem cells (SB623): a phase 1/2a study. J Neurosurg, 2018, 131(5): 1-11.
65.	Hess DC, Wechsler LR, Clark WM, et al. Safety and efficacy of multipotent adult progenitor cells in acute ischaemic stroke (MASTERS): a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol, 2017, 16(5): 360-368.
66.	Savitz SI, Misra V, Kasam M, et al. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann Neurol, 2011, 70(1): 59-69.
67.	Zhang G, Li Y, Reuss JL, et al. Stable intracerebral transplantation of neural stem cells for the treatment of paralysis due to ischemic stroke. Stem Cells Transl Med, 2019, 8(10): 999-1007.

1. Neuhaus AA, Couch Y, Hadley G, et al. Neuroprotection in stroke: the importance of collaboration and reproducibility. Brain, 2017, 140(8): 2079-2092.
2. Song S, Liang L, Fonarow GC, et al. Comparison of clinical care and in-hospital outcomes of Asian American and White Patients with acute ischemic stroke. JAMA Neurol, 2019, 76(4): 430-439.
3. Doeppner TR, Bähr M, Hermann DM, et al. Concise review: extracellular vesicles overcoming limitations of cell therapies in ischemic stroke. Stem Cells Transl Med, 2017, 6(11): 2044-2052.
4. Wardlaw JM, Murray V, Berge E, et al. Thrombolysis for acute ischaemic stroke. Cochrane Database Syst Rev, 2014, 7(4): Cd000213.
5. Liu X, Ye R, Yan T, et al. Cell based therapies for ischemic stroke: from basic science to bedside. Prog Neurobiol, 2014, 115: 92-115.
6. Bernstock JD, Peruzzotti-Jametti L, Ye D, et al. Neural stem cell transplantation in ischemic stroke: A role for preconditioning and cellular engineering. J Cereb Blood Flow Metab, 2017, 37(7): 2314-2319.
7. Zhang J, Chopp M. Cell-based therapy for ischemic stroke. Expert Opin Biol Ther, 2013, 13(9): 1229-1240.
8. Horie N, Pereira MP, Niizuma K, et al. Transplanted stem cell-secreted vascular endothelial growth factor effects poststroke recovery, inflammation, and vascular repair. Stem Cells, 2011, 29(2): 274-285.
9. Andres RH, Horie N, Slikker W, et al. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain, 2011, 134(Pt 6): 1777-1789.
10. Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature, 2005, 436(7048): 193-200.
11. Imitola J, Raddassi K, Park KI, et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A, 2004, 101(52): 18117-18122.
12. Yan YP, Sailor KA, Lang BT, et al. Monocyte chemoattractant protein-1 plays a critical role in neuroblast migration after focal cerebral ischemia. J Cereb Blood Flow Metab, 2007, 27(6): 1213-1224.
13. Horie N, Hiu T, Nagata I. Stem cell transplantation enhances endogenous brain repair after experimental stroke. Neurol Med Chir (Tokyo), 2015, 55(2): 107-112.
14. Sinden JD, Hicks C, Stroemer P, et al. Human neural stem cell therapy for chronic ischemic stroke: charting progress from laboratory to patients. Stem Cells Dev, 2017, 26(13): 933-947.
15. Aday S, Zoldan J, Besnier M, et al. Synthetic microparticles conjugated with VEGF₁₆₅ improve the survival of endothelial progenitor cells via microRNA-17 inhibition. Nat Commun, 2017, 8(1): 747.
16. Stonesifer C, Corey S, Ghanekar S, et al. Stem cell therapy for abrogating stroke-induced neuroinflammation and relevant secondary cell death mechanisms. Prog Neurobiol, 2017, 158: 94-131.
17. Loubinoux I, Demain B, Davoust C, et al. Stem cells and motor recovery after stroke. Ann Phys Rehabil Med, 2014, 57(8): 499-508.
18. Yamashita T, Liu W, Matsumura Y, et al. Novel therapeutic transplantation of induced neural stem cells for stroke. Cell Transplant, 2017, 26(3): 461-467.
19. Kubis N. Stroke and the cell therapy saga: towards a safe, swift and efficient utilization of cells. Keio J Med, 2017, 66(3): 55.
20. Tanaka E, Ogawa Y, Mukai T, et al. Dose-dependent effect of intravenous administration of human umbilical cord-derived mesenchymal stem cells in neonatal stroke mice. Front Neurol, 2018, 9: 133.
21. Lazarov O, Mattson MP, Peterson DA, et al. When neurogenesis encounters aging and disease. Trends Neurosci, 2010, 33(12): 569-579.
22. Wang F, Tang H, Zhu J, et al. Transplanting mesenchymal stem cells for treatment of ischemic stroke. Cell Transplant, 2018, 27(12): 1825-1834.
23. Huang L, Zhang L. Neural stem cell therapies and hypoxic-ischemic brain injury. Prog Neurobiol, 2019, 173: 1-17.
24. Jiang XC, Xiang JJ, Wu HH, et al. Neural stem cells transfected with reactive oxygen species-responsive polyplexes for effective treatment of ischemic stroke. Adv Mater, 2019, 31(10): e1807591.
25. Jiang Y, Wei N, Zhu J, et al. Effects of brain-derived neurotrophic factor on local inflammation in experimental stroke of rat. Mediators Inflamm, 2010, 2010: 372423.
26. Lee HJ, Lim IJ, Lee MC, et al. 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.
27. Hass R, Kasper C, Böhm S, et al. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC. Cell Commun Signal, 2011, 9(1): 12.
28. Huang P, Gebhart N, Richelson E, et al. Mechanism of mesenchymal stem cell-induced neuron recovery and anti-inflammation. Cytotherapy, 2014, 16(10): 1336-1344.
29. Gu N, Rao C, Tian Y, et al. Anti-inflammatory and antiapoptotic effects of mesenchymal stem cells transplantation in rat brain with cerebral ischemia. J Stroke Cerebrovasc Dis, 2014, 23(10): 2598-2606.
30. Wei L, Fraser JL, Lu ZY, et al. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis, 2012, 46(3): 635-645.
31. Liu K, Guo L, Zhou Z, et al. Mesenchymal stem cells transfer mitochondria into cerebral microvasculature and promote recovery from ischemic stroke. Microvasc Res, 2019, 123: 74-80.
32. Hayakawa K, Esposito E, Wang X, et al. Transfer of mitochondria from astrocytes to neurons after stroke. Nature, 2016, 535(7613): 551-555.
33. Sheikh AM, Yano S, Mitaki S, et al. A Mesenchymal stem cell line (B10) increases angiogenesis in a rat MCAO model. Exp Neurol, 2019, 311: 182-193.
34. Cheng Z, Wang L, Qu M, et al. Mesenchymal stem cells attenuate blood-brain barrier leakage after cerebral ischemia in mice. J Neuroinflammation, 2018, 15(1): 135.
35. Bühnemann C, Scholz A, Bernreuther C, et al. Neuronal differentiation of transplanted embryonic stem cell-derived precursors in stroke lesions of adult rats. Brain, 2006, 129(Pt 12): 3238-3248.
36. Wei L, Cui L, Snider BJ, et al. Transplantation of embryonic stem cells overexpressing Bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis, 2005, 19(1-2): 183-193.
37. Drury-Stewart D, Song M, Mohamad O, et al. Highly efficient differentiation of neural precursors from human embryonic stem cells and benefits of transplantation after ischemic stroke in mice. Stem Cell Res Ther, 2013, 4(4): 93.
38. Kosi N, Alić I, Salamon I, et al. Stroke promotes survival of nearby transplanted neural stem cells by decreasing their activation of caspase 3 while not affecting their differentiation. Neurosci Lett, 2018, 666: 111-119.
39. Zlokovic BV. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron, 2008, 57(2): 178-201.
40. Abbott NJ, Patabendige AA, Dolman DE, et al. Structure and function of the blood-brain barrier. Neurobiol Dis, 2010, 37(1): 13-25.
41. Daneman R, Prat A. The blood-brain barrier. Cold Spring Harb Perspect Biol, 2015, 7(1): a020412.
42. Stamatovic SM, Keep RF, Andjelkovic AV. Brain endothelial cell-cell junctions: how to “open” the blood brain barrier. Curr Neuropharmacol, 2008, 6(3): 179-192.
43. Pendharkar AV, Chua JY, Andres RH, et al. Biodistribution of neural stem cells after intravascular therapy for hypoxic-ischemia. Stroke, 2010, 41(9): 2064-2070.
44. Hersh DS, Wadajkar AS, Roberts N, et al. Evolving drug delivery strategies to overcome the blood brain barrier. Curr Pharm Des, 2016, 22(9): 1177-1193.
45. Jin K, Sun Y, Xie L, et al. Comparison of ischemia-directed migration of neural precursor cells after intrastriatal, intraventricular, or intravenous transplantation in the rat. Neurobiol Dis, 2005, 18(2): 366-374.
46. Sharp J, Keirstead HS. Stem cell-based cell replacement strategies for the central nervous system. Neurosci Lett, 2009, 456(3): 107-111.
47. Jiang Y, Zhu J, Xu G, et al. Intranasal delivery of stem cells to the brain. Expert Opin Drug Deliv, 2011, 8(5): 623-632.
48. Danielyan L, Schäfer R, von Ameln-Mayerhofer A, et al. Intranasal delivery of cells to the brain. Eur J Cell Biol, 2009, 88(6): 315-324.
49. Wilson EH, Weninger W, Hunter CA. Trafficking of immune cells in the central nervous system. J Clin Invest, 2010, 120(5): 1368-1379.
50. Liu L, Eckert MA, Riazifar H, et al. From blood to the brain: can systemically transplanted mesenchymal stem cells cross the blood-brain barrier? Stem Cells Int, 2013, 2013: 435093.
51. Teo GS, Ankrum JA, Martinelli R, et al. Mesenchymal stem cells transmigrate between and directly through tumor necrosis factor-α-activated endothelial cells via both leukocyte-like and novel mechanisms. Stem Cells, 2012, 30(11): 2472-2486.
52. Steingen C, Brenig F, Baumgartner L, et al. Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. J Mol Cell Cardiol, 2008, 44(6): 1072-1084.
53. Yilmaz G, Vital S, Yilmaz CE, et al. Selectin-mediated recruitment of bone marrow stromal cells in the postischemic cerebral microvasculature. Stroke, 2011, 42(3): 806-811.
54. Conaty P, Sherman LS, Naaldijk Y, et al. Methods of mesenchymal stem cell homing to the blood-brain barrier. Methods Mol Biol, 2018, 1842: 81-91.
55. Freeman WD. Management of intracranial pressure. Continuum (Minneap Minn), 2015, 21(5 Neurocritical Care): 1299-1323.
56. Gonzales-Portillo GS, Sanberg PR, Franzblau M, et al. Mannitol-enhanced delivery of stem cells and their growth factors across the blood-brain barrier. Cell Transplant, 2014, 23(4-5): 531-539.
57. Seyfried DM, Han Y, Yang D, et al. Mannitol enhances delivery of marrow stromal cells to the brain after experimental intracerebral hemorrhage. Brain Res, 2008, 1224: 12-19.
58. Shen WB, Anastasiadis P, Nguyen B, et al. Magnetic enhancement of stem cell-targeted delivery into the brain following MR-guided focused ultrasound for opening the blood-brain barrier. Cell Transplant, 2017, 26(7): 1235-1246.
59. Burgess A, Ayala-Grosso CA, Ganguly M, et al. Targeted delivery of neural stem cells to the brain using MRI-guided focused ultrasound to disrupt the blood-brain barrier. PLoS One, 2011, 6(11): e27877.
60. Wolburg H, Wolburg-Buchholz K, Engelhardt B. Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves tight junctions intact. Acta Neuropathol, 2005, 109(2): 181-190.
61. Prasad K, Sharma A, Garg A, et al. Intravenous autologous bone marrow mononuclear stem cell therapy for ischemic stroke: a multicentric, randomized trial. Stroke, 2014, 45(12): 3618-3624.
62. Banerjee S, Bentley P, Hamady M, et al. Intra-arterial immunoselected CD34+ stem cells for acute ischemic stroke. Stem Cells Transl Med, 2014, 3(11): 1322-1330.
63. Díez-Tejedor E, Gutiérrez-Fernández M, Martínez-Sánchez P, et al. 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.
64. Steinberg GK, Kondziolka D, Wechsler LR, et al. Two-year safety and clinical outcomes in chronic ischemic stroke patients after implantation of modified bone marrow-derived mesenchymal stem cells (SB623): a phase 1/2a study. J Neurosurg, 2018, 131(5): 1-11.
65. Hess DC, Wechsler LR, Clark WM, et al. Safety and efficacy of multipotent adult progenitor cells in acute ischaemic stroke (MASTERS): a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Neurol, 2017, 16(5): 360-368.
66. Savitz SI, Misra V, Kasam M, et al. Intravenous autologous bone marrow mononuclear cells for ischemic stroke. Ann Neurol, 2011, 70(1): 59-69.
67. Zhang G, Li Y, Reuss JL, et al. Stable intracerebral transplantation of neural stem cells for the treatment of paralysis due to ischemic stroke. Stem Cells Transl Med, 2019, 8(10): 999-1007.

Chinese Journal of Reparative and Reconstructive Surgery

Research progress of different types of stem cells in treatment of ischemic stroke

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