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Review

Intra-arterial administration of cell-based biological agents for ischemic stroke therapy

, , &
Pages 249-259 | Received 02 Oct 2018, Accepted 05 Jan 2019, Published online: 21 Jan 2019

References

  • Craig AJ, Housley GD. Evaluation of gene therapy as an intervention strategy to treat brain injury from stroke. Front Mol Neurosci. 2016;24(9):34.
  • de Los Ríos la Rosa F, Khoury J, Kissela BM, et al. Eligibility for intravenous recombinant tissue-type plasminogen activator within a population: the effect of the european cooperative acute stroke study (ECASS) III trial. Stroke. 2012;43(6):1591–1595.
  • Madsen TE, Khoury JC, Alwell KA, et al. Analysis of tissue plasminogen activator eligibility by sex in the Greater Cincinnati/Northern Kentucky stroke study. Stroke. 2015;46(3):717–721.
  • Emberson J, Lees KR, Lyden P, et al. Effect of treatment delay, age, and stroke severity on the effects of intravenous thrombolysis with alteplase for acute ischaemic stroke: a meta-analysis of individual patient data from randomised trials. Lancet. 2014 29;384(9958):1929–1935.
  • Saver JL, Goyal M, Bonafe A, et al. Stent-retriever thrombectomy after intravenous t-PA vs. t-PA alone in stroke. N Engl J Med. 2015;372(24):2285–2295.
  • Bliss T, Guzman R, Daadi M, et al. Cell transplantation therapy for stroke. Stroke. 2007;38:817–826.
  • Rhim T, Lee M. Targeted delivery of growth factors in ischemic stroke animal models. Expert Opin Drug Deliv. 2016;13(5):709–723.
  • Yanamoto H, Nagata I, Niitsu Y, et al. Evaluation of MCAO stroke models in normotensive rats: standardized neocortical infarction by the 3VO technique. Exp Neurol. 2003;182(2):261–274.
  • 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;4:93.
  • Mohamad O, Drury-Stewart D, Song M, et al. Vector-free and transgene-free human iPS cells differentiate into functional neurons and enhance functional recovery after ischemic stroke in mice. PLoS ONE. 2013;8(5):e64160.
  • Yuan T, Liao W, Feng NH, et al. Human induced pluripotent stem cell-derived neural stem cells survive, migrate, differentiate, and improve neurologic function in a rat model of middle cerebral artery occlusion. Stem Cell Res Ther. 2013;4(3):73.
  • He B, Yao Q, Liang Z, et al. The dose of intravenously transplanted bone marrow stromal cells determines the therapeutic effect on vascular remodeling in a rat model of ischemic stroke. Cell Transplant. 2016;25:2173–2185.
  • Lim J, Jeong C, Jun J, et al. Therapeutic effects of human umbilical cord blood-derived mesenchymal stem cells after intrathecal administration by lumbar puncture in a rat model of cerebral ischemia. Stem Cell Res Ther. 2011;2(5):38.
  • Zhu J, Liu Q, Jiang Y, et al. Enhanced angiogenesis promoted by human umbilical mesenchymal stem cell transplantation in stroked mouse is Notch1 signaling associated. Neuroscience. 2015;290:288–299.
  • Nomura T, Honmou O, Harada K, et al. I.V. infusion of brain-derived neurotrophic factor gene-modified human mesenchymal stem cells protects against injury in a cerebral ischemia model in adult rat. Neuroscience. 2005;136(1):161–169.
  • Liu H, Honmou O, Harada K, et al. Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain. 2006;129:2734–2745.
  • Chen Y, Zhu HB, Liao J, et al. Regulation of naotai recipe on the expression of HIF-lα/VEGF signaling pathway in cerebral ischemia/reperfusion rats. Zhongguo Zhong Xi Yi Jie He Za Zhi. 2014;34(10):1225–1230.
  • Rosell A, Cuadrado E, Ortega-Aznar A, et al. MMP-9 positive neutrophil infiltration is associated to blood-brain barrier breakdown and basal lamina type IV collagen degradation during hemorrhagic transformation after human ischemic stroke. Stroke. 2008;39:1121–1126.
  • Labrie M, St-Pierre Y. Epigenetic regulation of mmp-9 gene expression. Cell Mol Life Sci. 2013;70:3109–3124.
  • Chen YJ, Kuo CD, Chen SH, et al. Small-molecule synthetic compound norcantharidin reverses multi-drug resistance by regulating Sonic hedgehog signaling in human breast cancer cells. PLoS One. 2012;7(5):e37006.
  • Hacke W. A new dawn for imaging-based selection in the treatment of acute stroke. N Engl J Med. 2018;378(1):81–83.
  • Heiss WD. Ischemic penumbra: evidence from functional imaging in man. J Cereb Blood Flow Metab. 2000;20:1276–1293.
  • Misra V, Ritchie MM, Stone LL, et al. Stem cell therapy in ischemic stroke: role of IV and intra-arterial therapy. Neurology. 2012;79(13 suppl 1):S207–S212.
  • Lemmens R, Stenberg G. Stem cell therapy for acute cerebral injury: what do we know and what will the future bring? Curr Opin Neurol. 2013 Dec;26(6):617–625.
  • Guzman R, Janowski M, Walczak P. Intra-arterial delivery of cell therapies for stroke. Stroke. 2018;49(5):1075–1082.
  • Ballabh P, Braun A, Nedergaard M. The blood–brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis. 2004;16(1):1–13.
  • Khan IS, Odom M, Ehtesham M, et al. Intraarterial administration of norcantharidin attenuates ischemic stroke damage in rodents when given at the time of reperfusion: novel uses of endovascular capabilities. J Neurosurg. 2016;125(1):152–159.
  • Ferrara N, Houck K, Jakeman L, et al. Molecular and biological properties of the vascular endothelial growth factor family of proteins. Endocr.Rev. 1992;13(1):18–32.
  • Sondell M, Lundborg G, Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci. 1999;19(14):5731–5740.
  • Islamov RR, Chintalgattu V, Pak ES, et al. Induction of VEGF and its Flt-1 receptor after sciatic nerve crush injury. Neuroreport. 2004;15(13):2117–2121.
  • Jin L, Ne T, Blau CA. Marrow sensitization to 5-fluorouracil using the ligands for Flt-3 and c-Kit. Exp Hematol 1999;27(3):520–525.
  • Rosenstein JM, Mani N, Silverman WF, et al. Patterns of brain angiogenesis after vascular endothelial growth factor administration in vitro and in vivo. Proc Natl Acad Sci USA. 1998;95(12):7086–7091.
  • Cheng H, Wu JP, Tzeng SF. Neuroprotection of glial cell line derived neurotrophic factor in damaged spinal cords following contusive injury. J Neurosci Res. 2002;69(3):397–405.
  • Iannotti C, Li H, Yan P, et al. Glial cell line-derived neurotrophic factor-enriched bridging transplants promote propriospinal axonal regeneration and enhance myelination after spinal cord injury. Exp Neurol. 2003;183(2):379–393.
  • Karlupia N, Manley NC, Prasad K, et al. Intra-arterial transplantation of human umbilical cord blood mononuclearcells is more efficacious and safer compared with umbilical cord mesenchymal stromal cells in a rodent stroke model. Stem Cell Res Ther. 2014;5(2):45.
  • Jeong H, Yim HW, Cho Y, et al. Efficacy and safety of stem cell therapies for patients with stroke: a systematic review and single arm meta-analysis. Int J Stem Cells. 2014;7(2):63–69.
  • Wang XL, Zhao YS, Hu MY, et al. Umbilical cord blood cells regulate endogenous neural stem cell proliferation via hedgehog signaling in hypoxic ischemic neonatal rats. Brain Res. 2013;1518:26–35.
  • Chernykh ER, Shevela EY, Starostina NM, et al. Safety and therapeutic potential of M2 macrophages in stroke treatment. CellTransplant. 2016;25(8):1461–1471.
  • Islamov RR, Izmailov AA, Sokolov ME, et al. Evaluation of direct and cell-mediated triple-gene therapy in spinal cord injury in rats. Brain Res Bull. 2017;132:44–52.
  • Islamov RR, Rizvanov AA, Fedotova VY, et al. Tandem delivery of multiple therapeutic genes using umbilical cord blood cells improves symptomatic outcomes in ALS. Mol Neurobiol. 2017;54(6):4756–4763.
  • Yang WZ, Zhang Y, Wu F, et al. Safety evaluation of allogeneic umbilical cord blood mononuclear cell therapy for degenerative conditions. J Transl Med. 2010;8:75.
  • Ballen KK, Gluckman E, Broxmeyer HE. Umbilical cord blood transplantation: the first 25 years and beyond. Blood. 2013;122(4):491–498.
  • Weise G, Lorenz M, Pösel C, et al. Transplantation of cryopreserved human umbilical cord blood mononuclear cells does not induce sustained recovery after experimental stroke in spontaneously hypertensive rats. J Cereb Blood Flow Metab. 2014;34:182–184.
  • Boltze J, Reich DM, Hau S, et al. Assessment of neuroprotective effects of human umbilical cord blood mononuclear cell subpopulations in vitro and in vivo. Cell Transplant. 2012;21(4):723–737.
  • Chen J, Sanberg PR, Li Y, et al. Intravenous administration of human umbilical cord blood reduces behavioral deficits after stroke in rats. Stroke. 2001;32:2682–2688.
  • Sokolov ME, Bashirov FV, Markosyan VA, et al. Triple-gene therapy for stroke: a proof-of-concept in vivo study in rats front. Pharmacol. 2018;9:111.
  • Czabotar PE, Lessene G, Strasser A, et al. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Biol. 2014;15(1):49–63.
  • Zhong LT, Sarafian T, Kane DJ, et al. Bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci USA. 1993;90(10):4533–4537.
  • Murphy AN, Fiskum G. Bcl-2 and Ca(2+)-mediated mitochondrial dysfunction in neural cell death. Biochem Soc Symp. 1999;66:33–41.
  • Kane DJ, Sarafian TA, Anton R, et al. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science. 1993;262(5137):1274–1277.
  • Zhao H, Yenari M, Cheng D, et al. Bcl-2 transfection via herpes simplex virus blocks apoptosis-inducing factor translocation after focal ischemia in the rat. J Cereb Blood Flow Metab. 2004;24(6):681–692.
  • Kitagawa K, Matsumoto M, Tsujimoto Y, et al. Amelioration of hippocampal neuronal damage after global ischemia by neuronal overexpression of BCL-2 in transgenic mice. Stroke. 1998;29(12):2616–2621.
  • Lei ZN, Liu F, Zhang LM, et al. Bcl-2 increases stroke-induced striatal neurogenesis in adult brains by inhibiting BMP-4 function via activation of beta-catenin signaling. Neurochem Int. 2012;61(1):34–42.
  • van der Weerd L, Tariq Akbar M, Aron Badin R, et al. Overexpression of heat shock protein 27 reduces cortical damage after cerebral ischemia. J Cereb Blood Flow Metab. 2010;30(4):849–856.
  • Yenari MA, Fink SL, Sun GH, et al. Gene therapy with HSP72 is neuroprotective in rat models of stroke and epilepsy. Ann.Neurol. 1998;44(4):584–591.
  • Hoehn B, Ringer TM, Xu L, et al. Overexpression of HSP72 after induction of experimental stroke protects neurons from ischemic damage. J Cereb Blood Flow Metab. 2001;21(11):1303–1309.
  • Kelly S, Zhang ZJ, Zhao H, et al. Gene transfer of HSP72 protects cornu ammonis 1 region of the hippocampus neurons from global ischemia: influence of Bcl-2. Ann Neurol. 2002;52(2):160–167.
  • Badin RA, Lythgoe MF, van der Weerd L, et al. Neuroprotective effects of virally delivered HSPs in experimental stroke. J Cereb Blood Flow Metab. 2006;26(3):371–381.
  • Badin RA, Modo M, Cheetham M, et al. Protective eect of post-ischaemic viral delivery of heat shock proteins in vivo. J Cereb Blood Flow Metab. 2009;29(2):254–263.
  • Lawrence MS, McLaughlin JR, Sun GH, et al. Herpes simplex viral vectors expressing Bcl-2 are neuroprotective when delivered after a stroke. J Cereb Blood Flow Metab. 1997;17(7):740–744.
  • Otsuka S, Sakakima H, Sumizono M, et al. The neuroprotective effects of preconditioning exercise on brain damage and neurotrophic factors after focal brain ischemia in rats. Behav Brain Res. 2016;303:9–18.
  • Zhang Y, Pardridge WM. Neuroprotection in transient focal brain ischemia after delayed intravenous administration of brain-derived neurotrophic factor conjugated to a blood-brain barrier drug targeting system. Stroke. 2001;32(6):1378–1384.
  • Yuan M, Wen S, Yang C, et al. Transplantation of neural stem cells overexpressing glial cell line-derived neurotrophic factor enhances Akt and Erk1/2 signaling and neurogenesis in rats after stroke.Chin. Med J. 2013;126(7):1302–1309.
  • Semkova I, Krieglstein J. Neuroprotection mediated via neurotrophic factors and induction of neurotrophic factors. Brain Res Rev. 1999;30(2):176–188.
  • Tabakman R, Jiang H, Shahar I, et al. Neuroprotection by NGF in the PC12 in vitro OGD model: involvement of mitogen-activated protein kinases and gene expression. Ann NY Acad Sci. 2005;1053:84–96.
  • Andsberg G, Kokaia Z, Klein RL, et al. Neuropathological and behavioral consequences of adeno-associated viral vector-mediated continuous intrastriatal neurotrophin delivery in a focal ischemia model in rats. Neurobiol Dis. 2002;9(2):187–204.
  • Zhang J, Yu Z, Yu Z, et al. rAAV-mediated delivery of brain-derived neurotrophic factor promotes neurite outgrowth and protects neurodegeneration in focal ischemic model. Int J Clin Exp Pathol. 2011;4(5):496–504.
  • Tsai TH, Chen SL, Chiang YH, et al. Recombinant adeno-associated virus vector expressing glial cell linederived neurotrophic factor reduces ischemia-induced damage. Exp Neurol. 2000;166(2):266–275.
  • Tsai TH, Chen SL, Xiao X, et al. Gene therapy of focal cerebral ischemia using defective recombinant adeno-associated virus vectors. Front Biosci. 2006;11:2061–2070.
  • Hermann DM, Kilic E, Kugler S, et al. Adenovirus-mediated GDNF and CNTF pretreatment protects against striatal injury following transient middle cerebral artery occlusion in mice. Neurobiol Dis. 2001;8(4):655–666.
  • Zhang WR, Sato K, Iwai M, et al. Therapeutic time window of adenovirus-mediated GDNF gene transfer after transient middle cerebral artery occlusion in rat. Brain Res. 2002;947(1):140–145.
  • Harvey BK, Chang CF, Chiang YH, et al. HSV amplicon delivery of glial cell line-derived neurotrophic factor is neuroprotective against ischemic injury. Exp Neurol. 2003;183(1):47–55.
  • Wong LF, Ralph GS, Walmsley LE, et al. Lentiviral-mediated delivery of Bcl-2 or GDNF protects against excitotoxicity in the rat hippocampus. Mol Ther. 2005;11(1):89–95.
  • Matlik K, Abo-Ramadan U, Harvey BK, et al. AAV-mediated targeting of gene expression to the peri-infarct region in rat cortical stroke model. J Neurosci Methods. 2014 30;236:107–113.
  • Boltze J., Arnold A, Walczak P, et al. The dark side of the force – constraints and complications of cell therapies for stroke. Front Neurol. 2015;6:155.
  • Murakami K, Kondo T, Epstein CJ, et al. Overexpression of CuZn-Superoxide dismutase reduces hippocampal injury after global ischemia in transgenic mice. Stroke. 1997;28(9):1797–1804.
  • Chan PH, Kawase M, Murakami K, et al. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J Neurosci. 1998;18(20):8292–8299.
  • Kawase M, Murakami K, Fujimura M, et al. Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency. Stroke. 1999;30(9):1962–1968.
  • Moretti A, Ferrari F, Villa RF. Neuroprotection for ischemic stroke: current status and challenges. Pharmacol Ther. 2015;146:23–34.
  • García-Berrocoso T, Giralt D, Llombart V, et al. Chemokines after human ischemic stroke: from neurovascular unit to blood using protein arrays. Transl Proteom. 2014;3:1–9.
  • Wang Y, Huang J, Li Y, et al. Roles of chemokine CXCL12 and its receptors in ischemic stroke. Curr Drug Targets. 2012;13(2):166–172.
  • Ruscher K, Kuric E, Liu Y, et al. Inhibition of CXCL12 signaling attenuates the postischemic immune response and improves functional recovery after stroke. J Cereb Blood Flow Metab. 2013;33(8):1225–1234.
  • Tsai TH, Chen SL, Xiao X, et al. Gene treatment of cerebral stroke by rAAV vector delivering IL-1ra in a rat model. Neuroreport. 2003;14(6):803–807.
  • Bowen KK, Dempsey RJ, Vemuganti R. Adult interleukin-6 knockout mice show compromised neurogenesis. Neuroreport. 2011;22(3):126–130.
  • Gonzalez-Perez O, Gutierrez-Fernandez F, Lopez-Virgen V, et al. Immunological regulation of neurogenic niches in the adult brain. Neuroscience. 2012;226(8):270–281.
  • Wang Q, Tang XN, Yenari MA. The inflammatory response in stroke. J Neuroimmunol. 2007;184(1–2):53–68.
  • Mennicken F, Maki R, de Souza EB, et al. Chemokines and chemokine receptors in the CNS: a possible role in neuroinflammation and patterning. Trends Pharmacol Sci. 1999;20(2):73–78.
  • Bajetto A, Bonavia R, Barbero S, et al. Chemokines and their receptors in the central nervous system. Front Neuroendocrinol. 2001;22(3):147–184.
  • Janowski M, Lyczek A, Engels C, et al. Cell size and velocity of injection are major determinants of the safety of intracarotid stem cell transplantation. J Cereb Blood Flow Metab. 2013;33:921–927.
  • Cui LL, Kerkelä E, Bakreen A, et al. The cerebral embolism evoked by intra-arterial delivery of allogeneic bone marrow mesenchymal stem cells in rats is related to cell dose and infusion velocity. Stem Cell Res Ther. 2015;6:11.
  • Cui LL, Nitzsche F, Pryazhnikov E, et al. Integrin α4 overexpression on rat mesenchymal stem cells enhances transmigration and reduces cerebral embolism after intracarotid injection. Stroke. 2017 Oct;48(10):2895–2900.
  • Da Fonseca LMB, Gutfilen B, Rosado de Castro PH, et al. Migration and homing of bone-marrow mononuclear cells in chronic ischemic stroke after intra-arterial injection. Exp Neurol. 2010;221:122–128.
  • Rosadode-Castro P-H, Schmidt FR, Battistella V, et al. Biodistribution of bone marrow mononuclear cells after intra-arterial or intravenous transplantation in subacute stroke patients. Regener Med. 2013;8(2):145–155.
  • Barbosa Da Fonseca LM, Battistella V, de Freitas GR, et al. Early tissue distribution of bone marrow mononuclear cells after intra-arterial delivery in a patient with chronic stroke. Circulation. 2009;120(6):539–541.
  • Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron. 2010;67(2):181–198.
  • Campbell BC, Mitchell PJ. EXTEND-IA investigators. Endovascular therapy for ischemic stroke. N Engl J Med. 2015;372(24):2365–2366.
  • Nogueira RG, Jadhav AP, Haussen DC, et al. DAWN trial investigators. Thrombectomy 6 to 24 hours after stroke with a mismatch between deficit and infarct. N Engl J Med. 2018;378(1):11–21.
  • van Overhagen H, van Zwam WH, Krajina A, et al. CIRSE Position statement: interventional radiologists and intra-arterial stroke therapy. Cardiovasc Intervent Radiol. 2018;41(10):1460–1462.

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