Combining Growth Factor and Stem Cell Therapy for Stroke Rehabilitation, A Review

Author(s): Samira Asgharzade, Andisheh Talaei, Tahereh Farkhondeh, Fatemeh Forouzanfar*

Journal Name: Current Drug Targets

Volume 21 , Issue 8 , 2020


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Graphical Abstract:


Abstract:

Stroke is a serious, life-threatening condition demanding vigorous search for new therapies. Recent research has focused on stem cell-based therapies as a viable choice following ischemic stroke, based on studies displaying that stem cells transplanted to the brain not only survive but also cause functional recovery. Growth factors defined as polypeptides that regulate the growth and differentiation of many cell types. Many studies have demonstrated that combined use of growth factors may increase results by the stimulation of endogenous neurogenesis, anti-inflammatory, neuroprotection properties, and enhancement of stem cell survival rates and so may be more effective than a single stem cell therapy. This paper reviews and discusses the most promising new stroke recovery research, including combination treatment.

Keywords: Stem cell-based therapies, growth factors, oxidative stress, stroke, combination therapies, polypeptides.

[1]
Mozaffarian D, Benjamin EJ, Go AS, et al. Executive summary: heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation 2016; 133(4): 447-54.
[http://dx.doi.org/10.1161/CIR.0000000000000366] [PMID: 26811276]
[2]
Benjamin EJ, Virani SS, Callaway CW, et al. Heart disease and stroke statistics-2018 update: a report from the American Heart Association. Circulation 2018; 137(12): e67-e492.
[http://dx.doi.org/10.1161/CIR.0000000000000558] [PMID: 29386200]
[3]
Detante O, Rome C, Papassin J. How to use stem cells for repair in stroke patients. Rev Neurol (Paris) 2017; 173(9): 572-6.
[http://dx.doi.org/10.1016/j.neurol.2017.09.003] [PMID: 29033030]
[4]
Rhim T, Lee M. Targeted delivery of growth factors in ischemic stroke animal models. Expert Opin Drug Deliv 2016; 13(5): 709-23.
[http://dx.doi.org/10.1517/17425247.2016.1144588] [PMID: 26788902]
[5]
Forouzanfar F, Amin B, Ghorbani A, et al. New approach for the treatment of neuropathic pain: Fibroblast growth factor 1 gene-transfected adipose-derived mesenchymal stem cells. Eur J Pain 2018; 22(2): 295-310.
[http://dx.doi.org/10.1002/ejp.1119] [PMID: 28949091]
[6]
Cooke MJ, Wang Y, Morshead CM, Shoichet MS. Controlled epi-cortical delivery of epidermal growth factor for the stimulation of endogenous neural stem cell proliferation in stroke-injured brain. Biomaterials 2011; 32(24): 5688-97.
[http://dx.doi.org/10.1016/j.biomaterials.2011.04.032] [PMID: 21550655]
[7]
Ghazavi H, Hoseini SJ, Ebrahimzadeh-Bideskan A, et al. Fibroblast growth factor type 1 (FGF1)-overexpressed adipose-derived mesenchaymal stem cells (AD-MSCFGF1) induce neuroprotection and functional recovery in a rat stroke model. Stem Cell Rev Rep 2017; 13(5): 670-85.
[http://dx.doi.org/10.1007/s12015-017-9755-z] [PMID: 28795363]
[8]
Lee HJ, Lim IJ, Lee MC, Kim SU. 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): 3282-94.
[http://dx.doi.org/10.1002/jnr.22474] [PMID: 20818776]
[9]
Doyle KP, Simon RP, Stenzel-Poore MP. Mechanisms of ischemic brain damage. Neuropharmacology 2008; 55(3): 310-8.
[http://dx.doi.org/10.1016/j.neuropharm.2008.01.005] [PMID: 18308346]
[10]
Choi DW, Rothman SM. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu Rev Neurosci 1990; 13(1): 171-82.
[http://dx.doi.org/10.1146/annurev.ne.13.030190.001131] [PMID: 1970230]
[11]
Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010; 67(2): 181-98.
[http://dx.doi.org/10.1016/j.neuron.2010.07.002] [PMID: 20670828]
[12]
Dehbandi S, Speckmann EJ, Pape HC, Gorji A. Cortical spreading depression modulates synaptic transmission of the rat lateral amygdala. Eur J Neurosci 2008; 27(8): 2057-65.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06188.x] [PMID: 18412626]
[13]
Ekdahl CT, Kokaia Z, Lindvall O. Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 2009; 158(3): 1021-9.
[http://dx.doi.org/10.1016/j.neuroscience.2008.06.052] [PMID: 18662748]
[14]
Kettenmann H, Hanisch U-K, Noda M, Verkhratsky A. Physiology of microglia. Physiol Rev 2011; 91(2): 461-553.
[http://dx.doi.org/10.1152/physrev.00011.2010] [PMID: 21527731]
[15]
Kato H, Takahashi A, Itoyama Y. Cell cycle protein expression in proliferating microglia and astrocytes following transient global cerebral ischemia in the rat. Brain Res Bull 2003; 60(3): 215-21.
[http://dx.doi.org/10.1016/S0361-9230(03)00036-4] [PMID: 12754083]
[16]
Lucas SM, Rothwell NJ, Gibson RM. The role of inflammation in CNS injury and disease. Br J Pharmacol 2006; 147(S1)(Suppl. 1): S232-40.
[http://dx.doi.org/10.1038/sj.bjp.0706400] [PMID: 16402109]
[17]
Bigham A, Shadkhast M, Hassanpour H, Lakzian A, Khalegi M, Asgharzade S. Nitric oxide metabolite levels during the ectopic osteoinduction in rats. Comp Clin Pathol 2009; 18(4): 377-81.
[http://dx.doi.org/10.1007/s00580-009-0821-z]
[18]
Gao H-M, Hong J-S. Why neurodegenerative diseases are progressive: uncontrolled inflammation drives disease progression. Trends Immunol 2008; 29(8): 357-65.
[http://dx.doi.org/10.1016/j.it.2008.05.002] [PMID: 18599350]
[19]
Shichita T, Sugiyama Y, Ooboshi H, et al. Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med 2009; 15(8): 946-50.
[http://dx.doi.org/10.1038/nm.1999] [PMID: 19648929]
[20]
Ferrarese C, Mascarucci P, Zoia C, et al. Increased cytokine release from peripheral blood cells after acute stroke. J Cereb Blood Flow Metab 1999; 19(9): 1004-9.
[http://dx.doi.org/10.1097/00004647-199909000-00008] [PMID: 10478652]
[21]
Kumai Y, Ooboshi H, Takada J, et al. Anti-monocyte chemoattractant protein-1 gene therapy protects against focal brain ischemia in hypertensive rats. J Cereb Blood Flow Metab 2004; 24(12): 1359-68.
[http://dx.doi.org/10.1097/01.WCB.0000143534.76388.3C] [PMID: 15625410]
[22]
Yilmaz G, Granger DN. Cell adhesion molecules and ischemic stroke. Neurol Res 2008; 30(8): 783-93.
[http://dx.doi.org/10.1179/174313208X341085] [PMID: 18826804]
[23]
Frijns CJ, Kappelle LJ. Inflammatory cell adhesion molecules in ischemic cerebrovascular disease. Stroke 2002; 33(8): 2115-22.
[http://dx.doi.org/10.1161/01.STR.0000021902.33129.69] [PMID: 12154274]
[24]
Asahi M, Wang X, Mori T, et al. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 2001; 21(19): 7724-32.
[http://dx.doi.org/10.1523/JNEUROSCI.21-19-07724.2001] [PMID: 11567062]
[25]
Nibuya M, Morinobu S, Duman RS. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 1995; 15(11): 7539-47.
[http://dx.doi.org/10.1523/JNEUROSCI.15-11-07539.1995] [PMID: 7472505]
[26]
Kapadia R, Yi J-H, Vemuganti R. Mechanisms of antiinflammatory and neuroprotective actions of PPAR-gamma agonists. Frontiers in bioscience: a journal and virtual library 2008;; 13: 1813.
[27]
Echeverría F, Valenzuela R, Espinosa A, et al. Reduction of high-fat diet-induced liver proinflammatory state by eicosapentaenoic acid plus hydroxytyrosol supplementation: involvement of resolvins RvE1/2 and RvD1/2. J Nutr Biochem 2019; 63: 35-43.
[http://dx.doi.org/10.1016/j.jnutbio.2018.09.012] [PMID: 30321750]
[28]
Contreras AV, Torres N, Tovar AR. PPAR-α as a key nutritional and environmental sensor for metabolic adaptation. Adv Nutr 2013; 4(4): 439-52.
[http://dx.doi.org/10.3945/an.113.003798] [PMID: 23858092]
[29]
Chang C-Y, Kuan Y-H, Li J-R, et al. Docosahexaenoic acid reduces cellular inflammatory response following permanent focal cerebral ischemia in rats. J Nutr Biochem 2013; 24(12): 2127-37.
[http://dx.doi.org/10.1016/j.jnutbio.2013.08.004] [PMID: 24139673]
[30]
Echeverría F, Ortiz M, Valenzuela R, Videla LA. Long-chain polyunsaturated fatty acids regulation of PPARs, signaling: Relationship to tissue development and aging. Prostaglandins Leukot Essent Fatty Acids 2016; 114: 28-34.
[http://dx.doi.org/10.1016/j.plefa.2016.10.001] [PMID: 27926461]
[31]
Hernández-Rodas MC, Valenzuela R, Echeverría F, et al. supplementation with docosahexaenoic acid and extra virgin olive oil prevents liver steatosis induced by a high-fat diet in mice through ppar-α and nrf2 upregulation with concomitant srebp-1c and nf-kb downregulation. Mol Nutr Food Res 2017; 61(12)1700479
[http://dx.doi.org/10.1002/mnfr.201700479] [PMID: 28940752]
[32]
Chen H, Yoshioka H, Kim GS, Jung JE, Okami N, Sakata H, et al. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotectionAntioxidants & redox signaling 2011; 14((8):): 1505--17.
[http://dx.doi.org/10.1089/ars.2010.3576]
[33]
Asgharzade S, Rabiei Z, Rafieian-Kopaei M. Effects of Matricaria chamomilla extract on motor coordination impairment induced by scopolamine in rats. Asian Pac J Trop Biomed 2015; 5(10): 829-33.
[http://dx.doi.org/10.1016/j.apjtb.2015.06.006]
[34]
Alfieri A, Srivastava S, Siow RC, Modo M, Fraser PA, Mann GE. Targeting the Nrf2-Keap1 antioxidant defence pathway for neurovascular protection in stroke. J Physiol 2011; 589(17): 4125-36.
[http://dx.doi.org/10.1113/jphysiol.2011.210294] [PMID: 21646410]
[35]
Valenzuela R, Illesca P, Echeverría F, et al. Molecular adaptations underlying the beneficial effects of hydroxytyrosol in the pathogenic alterations induced by a high-fat diet in mouse liver: PPAR-α and Nrf2 activation, and NF-κB down-regulation. Food Funct 2017; 8(4): 1526-37.
[http://dx.doi.org/10.1039/C7FO00090A] [PMID: 28386616]
[36]
Echeverría F, Ortiz M, Valenzuela R, Videla LA. Hydroxytyrosol and cytoprotection: a projection for clinical interventions. Int J Mol Sci 2017; 18(5): 930.
[http://dx.doi.org/10.3390/ijms18050930] [PMID: 28452954]
[37]
Illesca P, Valenzuela R, Espinosa A, et al. Hydroxytyrosol supplementation ameliorates the metabolic disturbances in white adipose tissue from mice fed a high-fat diet through recovery of transcription factors Nrf2, SREBP-1c, PPAR-γ and NF-κB. Biomed Pharmacother 2019; 109: 2472-81.
[http://dx.doi.org/10.1016/j.biopha.2018.11.120] [PMID: 30551508]
[38]
Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407(6805): 770-6.
[http://dx.doi.org/10.1038/35037710] [PMID: 11048727]
[39]
MacManus JP, Buchan AM. Apoptosis after experimental stroke: fact or fashion? J Neurotrauma 2000; 17(10): 899-914.
[http://dx.doi.org/10.1089/neu.2000.17.899] [PMID: 11063056]
[40]
Hu Y, Deng H, Xu S, Zhang J. MicroRNAs regulate mitochondrial function in cerebral ischemia-reperfusion injury. Int J Mol Sci 2015; 16(10): 24895-917.
[http://dx.doi.org/10.3390/ijms161024895] [PMID: 26492239]
[41]
Niizuma K, Endo H, Nito C, Myer DJ, Chan PH. Potential role of PUMA in delayed death of hippocampal CA1 neurons after transient global cerebral ischemia. Stroke 2009; 40(2): 618-25.
[http://dx.doi.org/10.1161/STROKEAHA.108.524447] [PMID: 19095966]
[42]
Khoshnam SE, Winlow W, Farzaneh M. The Interplay of MicroRNAs in the Inflammatory Mechanisms Following Ischemic Stroke. J Neuropathol Exp Neurol 2017; 76(7): 548-61.
[http://dx.doi.org/10.1093/jnen/nlx036] [PMID: 28535304]
[43]
Maienschein J. Regenerative medicine’s historical roots in regeneration, transplantation, and translation. Dev Biol 2011; 358(2): 278-84.
[http://dx.doi.org/10.1016/j.ydbio.2010.06.014] [PMID: 20561516]
[44]
Biehl JK, Russell B. Introduction to stem cell therapy. J Cardiovasc Nurs 2009; 24(2): 98-103.
[http://dx.doi.org/10.1097/JCN.0b013e318197a6a5] [PMID: 19242274]
[45]
Naderi-Meshkin H, Bahrami AR, Bidkhori HR, Mirahmadi M, Ahmadiankia N. Strategies to improve homing of mesenchymal stem cells for greater efficacy in stem cell therapy. Cell Biol Int 2015; 39(1): 23-34.
[http://dx.doi.org/10.1002/cbin.10378] [PMID: 25231104]
[46]
Sanberg PR. Neural stem cells for Parkinson’s disease: to protect and repair. Proc Natl Acad Sci USA 2007; 104(29): 11869-70.
[http://dx.doi.org/10.1073/pnas.0704704104] [PMID: 17620601]
[47]
Weiss ML, Medicetty S, Bledsoe AR, et al. Human umbilical cord matrix stem cells: preliminary characterization and effect of transplantation in a rodent model of Parkinson’s disease. Stem Cells 2006; 24(3): 781-92.
[http://dx.doi.org/10.1634/stemcells.2005-0330] [PMID: 16223852]
[48]
Barami K, Diaz FG. Cellular transplantation and spinal cord injury. Neurosurgery 2000; 47(3): 691-700.
[PMID: 10981757]
[49]
Keirstead HS, Nistor G, Bernal G, et al. Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 2005; 25(19): 4694-705.
[http://dx.doi.org/10.1523/JNEUROSCI.0311-05.2005] [PMID: 15888645]
[50]
Teng YD, Lavik EB, Qu X, et al. Functional recovery following traumatic spinal cord injury mediated by a unique polymer scaffold seeded with neural stem cells. Proc Natl Acad Sci USA 2002; 99(5): 3024-9.
[http://dx.doi.org/10.1073/pnas.052678899] [PMID: 11867737]
[51]
Karussis D, Karageorgiou C, Vaknin-Dembinsky A, et al. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010; 67(10): 1187-94.
[http://dx.doi.org/10.1001/archneurol.2010.248] [PMID: 20937945]
[52]
Muraro PA, Douek DC, Packer A, et al. Thymic output generates a new and diverse TCR repertoire after autologous stem cell transplantation in multiple sclerosis patients. J Exp Med 2005; 201(5): 805-16.
[http://dx.doi.org/10.1084/jem.20041679] [PMID: 15738052]
[53]
Fassas A, Anagnostopoulos A, Kazis A, et al. Peripheral blood stem cell transplantation in the treatment of progressive multiple sclerosis: first results of a pilot study. Bone Marrow Transplant 1997; 20(8): 631-8.
[http://dx.doi.org/10.1038/sj.bmt.1700944] [PMID: 9383225]
[54]
Lee JS, Hong JM, Moon GJ, Lee PH, Ahn YH, Bang OY. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 2010; 28(6): 1099-106.
[http://dx.doi.org/10.1002/stem.430] [PMID: 20506226]
[55]
Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 2005; 57(6): 874-82.
[http://dx.doi.org/10.1002/ana.20501] [PMID: 15929052]
[56]
Stonesifer C, Corey S, Ghanekar S, Diamandis Z, Acosta SA, Borlongan CV. Stem cell therapy for abrogating stroke-induced neuroinflammation and relevant secondary cell death mechanisms. Prog Neurobiol 2017; 158: 94-131.
[http://dx.doi.org/10.1016/j.pneurobio.2017.07.004] [PMID: 28743464]
[57]
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): 378-87.
[http://dx.doi.org/10.1007/s12975-016-0482-6] [PMID: 27384771]
[58]
Yun Y-R, Won JE, Jeon E, et al. Fibroblast growth factors: biology, function, and application for tissue regeneration. J Tissue Eng 2010; 2010(1)218142
[http://dx.doi.org/10.4061/2010/218142] [PMID: 21350642]
[59]
Cairns K, Finklestein SP. Growth factors and stem cells as treatments for stroke recovery. Phys Med Rehabil Clin N Am 2003; 14(1)(Suppl.): S135-42.
[http://dx.doi.org/10.1016/S1047-9651(02)00059-1] [PMID: 12625643]
[60]
Kolb B, Morshead C, Gonzalez C, et al. Growth factor-stimulated generation of new cortical tissue and functional recovery after stroke damage to the motor cortex of rats. J Cereb Blood Flow Metab 2007; 27(5): 983-97.
[http://dx.doi.org/10.1038/sj.jcbfm.9600402] [PMID: 16985505]
[61]
Dempsey RJ, Sailor KA, Bowen KK, Türeyen K, Vemuganti R. Stroke-induced progenitor cell proliferation in adult spontaneously hypertensive rat brain: effect of exogenous IGF-1 and GDNF. J Neurochem 2003; 87(3): 586-97.
[http://dx.doi.org/10.1046/j.1471-4159.2003.02022.x] [PMID: 14535942]
[62]
Teramoto T, Qiu J, Plumier J-C, Moskowitz MA. EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia. J Clin Invest 2003; 111(8): 1125-32.
[http://dx.doi.org/10.1172/JCI200317170] [PMID: 12697732]
[63]
Wada K, Sugimori H, Bhide PG, Moskowitz MA, Finklestein SP. Effect of basic fibroblast growth factor treatment on brain progenitor cells after permanent focal ischemia in rats. Stroke 2003; 34(11): 2722-8.
[http://dx.doi.org/10.1161/01.STR.0000094421.61917.71] [PMID: 14576381]
[64]
Beilharz EJ, Russo VC, Butler G, et al. Co-ordinated and cellular specific induction of the components of the IGF/IGFBP axis in the rat brain following hypoxic-ischemic injury. Brain Res Mol Brain Res 1998; 59(2): 119-34.
[http://dx.doi.org/10.1016/S0169-328X(98)00122-3] [PMID: 9729323]
[65]
Wong RWC, Guillaud L. The role of epidermal growth factor and its receptors in mammalian CNS. Cytokine Growth Factor Rev 2004; 15(2-3): 147-56.
[http://dx.doi.org/10.1016/j.cytogfr.2004.01.004] [PMID: 15110798]
[66]
Lanfranconi S, Locatelli F, Corti S, et al. Growth factors in ischemic stroke. J Cell Mol Med 2011; 15(8): 1645-87.
[http://dx.doi.org/10.1111/j.1582-4934.2009.00987.x] [PMID: 20015202]
[67]
Arsenijevic Y, Weiss S, Schneider B, Aebischer P. Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci 2001; 21(18): 7194-202.
[http://dx.doi.org/10.1523/JNEUROSCI.21-18-07194.2001] [PMID: 11549730]
[68]
Schuldiner M, Yanuka O, Itskovitz-Eldor J, Melton DA, Benvenisty N. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc Natl Acad Sci USA 2000; 97(21): 11307-12.
[http://dx.doi.org/10.1073/pnas.97.21.11307] [PMID: 11027332]
[69]
Shen LH, Li Y, Chen J, et al. Therapeutic benefit of bone marrow stromal cells administered 1 month after stroke. J Cereb Blood Flow Metab 2007; 27(1): 6-13.
[http://dx.doi.org/10.1038/sj.jcbfm.9600311] [PMID: 16596121]
[70]
Teixeira FG, Carvalho MM, Sousa N, Salgado AJ. Mesenchymal stem cells secretome: a new paradigm for central nervous system regeneration? Cell Mol Life Sci 2013; 70(20): 3871-82.
[http://dx.doi.org/10.1007/s00018-013-1290-8] [PMID: 23456256]
[71]
Hsieh J-Y, Wang H-W, Chang S-J, et al. Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS One 2013; 8(8)e72604
[http://dx.doi.org/10.1371/journal.pone.0072604] [PMID: 23991127]
[72]
Moisan A, Favre I, Rome C, et al. Intravenous injection of clinical grade human MSCs after experimental stroke: functional benefit and microvascular effect. Cell Transplant 2016; 25(12): 2157-71.
[http://dx.doi.org/10.3727/096368916X691132] [PMID: 26924704]
[73]
Li Y, McIntosh K, Chen J, et al. Allogeneic bone marrow stromal cells promote glial-axonal remodeling without immunologic sensitization after stroke in rats. Exp Neurol 2006; 198(2): 313-25.
[http://dx.doi.org/10.1016/j.expneurol.2005.11.029] [PMID: 16455080]
[74]
Chen J, Shehadah A, Pal A, et al. Neuroprotective effect of human placenta-derived cell treatment of stroke in rats. Cell Transplant 2013; 22(5): 871-9.
[http://dx.doi.org/10.3727/096368911X637380] [PMID: 22469567]
[75]
Meirelles LdaS, Fontes AM, Covas DT, Caplan AI. Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 2009; 20(5-6): 419-27.
[http://dx.doi.org/10.1016/j.cytogfr.2009.10.002] [PMID: 19926330]
[76]
Sheikh AM, Nagai A, Wakabayashi K, et al. Mesenchymal stem cell transplantation modulates neuroinflammation in focal cerebral ischemia: contribution of fractalkine and IL-5. Neurobiol Dis 2011; 41(3): 717-24.
[http://dx.doi.org/10.1016/j.nbd.2010.12.009] [PMID: 21168500]
[77]
Ohtaki H, Ylostalo JH, Foraker JE, et al. Stem/progenitor cells from bone marrow decrease neuronal death in global ischemia by modulation of inflammatory/immune responses. Proc Natl Acad Sci USA 2008; 105(38): 14638-43.
[http://dx.doi.org/10.1073/pnas.0803670105] [PMID: 18794523]
[78]
Jin R, Liu L, Zhang S, Nanda A, Li G. Role of inflammation and its mediators in acute ischemic stroke. J Cardiovasc Transl Res 2013; 6(5): 834-51.
[http://dx.doi.org/10.1007/s12265-013-9508-6] [PMID: 24006091]
[79]
Kenmuir CL, Wechsler LR. Update on cell therapy for stroke. Stroke Vasc Neurol 2017; 2(2): 59-64.
[http://dx.doi.org/10.1136/svn-2017-000070] [PMID: 28959493]
[80]
Vu Q, Xie K, Eckert M, Zhao W, Cramer SC. Meta-analysis of preclinical studies of mesenchymal stromal cells for ischemic stroke. Neurology 2014; 82(14): 1277-86.
[http://dx.doi.org/10.1212/WNL.0000000000000278] [PMID: 24610327]
[81]
Hui Q, Jin Z, Li X, Liu C, Wang X. FGF family: from drug development to clinical application. Int J Mol Sci 2018; 19(7): 1875.
[http://dx.doi.org/10.3390/ijms19071875] [PMID: 29949887]
[82]
Ornitz DM, Xu J, Colvin JS, et al. Receptor specificity of the fibroblast growth factor family. J Biol Chem 1996; 271(25): 15292-7.
[http://dx.doi.org/10.1074/jbc.271.25.15292] [PMID: 8663044]
[83]
Distribution of acidic and basic fibroblast growth factors in the mature, injured and developing rat nervous system.Eckenstein FP,Andersson C, Kuzis K, Woodward WR. Progress in b rain research 1994; 103: pp 55-64.
[http://dx.doi.org/10.1016/S0079-6123(08)61126-7]
[84]
Rodriguez-Enfedaque A, Bouleau S, Laurent M, et al. FGF1 nuclear translocation is required for both its neurotrophic activity and its p53-dependent apoptosis protection. Biochim Biophys Acta 2009; 1793(11): 1719-27.
[http://dx.doi.org/10.1016/j.bbamcr.2009.09.010] [PMID: 19765618]
[85]
Bouleau S, Pârvu-Ferecatu I, Rodriguez-Enfedaque A, et al. Fibroblast Growth Factor 1 inhibits p53-dependent apoptosis in PC12 cells. Apoptosis 2007; 12(8): 1377-87.
[http://dx.doi.org/10.1007/s10495-007-0072-x] [PMID: 17473910]
[86]
Hoseini SJ, Ghazavi H, Forouzanfar F, et al. Fibroblast growth factor 1-transfected adipose-derived mesenchymal stem cells promote angiogenic proliferation. DNA Cell Biol 2017; 36(5): 401-12.
[http://dx.doi.org/10.1089/dna.2016.3546] [PMID: 28281780]
[87]
Ye L-B, Yu X-C, Xia Q-H, et al. Regulation of caveolin-1 and junction proteins by bFGF contributes to the integrity of blood–spinal cord barrier and functional recovery. Neurotherapeutics 2016; 13(4): 844-58.
[http://dx.doi.org/10.1007/s13311-016-0437-3] [PMID: 27170156]
[88]
Qian X, Davis AA, Goderie SK, Temple S. FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron 1997; 18(1): 81-93.
[http://dx.doi.org/10.1016/S0896-6273(01)80048-9] [PMID: 9010207]
[89]
Palmer TD, Ray J, Gage FH. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 1995; 6(5): 474-86.
[http://dx.doi.org/10.1006/mcne.1995.1035] [PMID: 8581317]
[90]
Zhang J-J, Zhu J-J, Hu Y-B, et al. Transplantation of bFGF-expressing neural stem cells promotes cell migration and functional recovery in rat brain after transient ischemic stroke. Oncotarget 2017; 8(60): 102067-77.
[http://dx.doi.org/10.18632/oncotarget.22155] [PMID: 29254225]
[91]
Knapp PE, Adams MH. Epidermal growth factor promotes oligodendrocyte process formation and regrowth after injury. Exp Cell Res 2004; 296(2): 135-44.
[http://dx.doi.org/10.1016/j.yexcr.2004.02.007] [PMID: 15149844]
[92]
Perez-Saad H, Subiros N, Berlanga J, Aldana L, Garcia Del Barco D. Neuroprotective effect of epidermal growth factor in experimental acrylamide neuropathy: an electrophysiological approach. J Peripher Nerv Syst 2017; 22(2): 106-11.
[http://dx.doi.org/10.1111/jns.12214] [PMID: 28436077]
[93]
Hebert TL, Wu X, Yu G, et al. Culture effects of epidermal growth factor (EGF) and basic fibroblast growth factor (bFGF) on cryopreserved human adipose-derived stromal/stem cell proliferation and adipogenesis. J Tissue Eng Regen Med 2009; 3(7): 553-61.
[http://dx.doi.org/10.1002/term.198] [PMID: 19670348]
[94]
Zhang ZG, Zhang L, Tsang W, et al. Correlation of VEGF and angiopoietin expression with disruption of blood-brain barrier and angiogenesis after focal cerebral ischemia. J Cereb Blood Flow Metab 2002; 22(4): 379-92.
[http://dx.doi.org/10.1097/00004647-200204000-00002] [PMID: 11919509]
[95]
Han J, Calvo CF, Kang TH, et al. Vascular endothelial growth factor receptor 3 controls neural stem cell activation in mice and humans. Cell Rep 2015; 10(7): 1158-72.
[http://dx.doi.org/10.1016/j.celrep.2015.01.049] [PMID: 25704818]
[96]
Chu K, Park K-I, Lee S-T, et al. Combined treatment of vascular endothelial growth factor and human neural stem cells in experimental focal cerebral ischemia. Neurosci Res 2005; 53(4): 384-90.
[http://dx.doi.org/10.1016/j.neures.2005.08.010] [PMID: 16198014]
[97]
Zhu W, Mao Y, Zhao Y, et al. Transplantation of vascular endothelial growth factor-transfected neural stem cells into the rat brain provides neuroprotection after transient focal cerebral ischemia. Neurosurgery 2005; 57(2): 325-33.
[http://dx.doi.org/10.1227/01.NEU.0000166682.50272.BC] [PMID: 16094163]
[98]
Lee HJ, Kim KS, Park IH, Kim SU. 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]
[99]
Bible E, Qutachi O, Chau DY, Alexander MR, Shakesheff KM, Modo M. Neo-vascularization of the stroke cavity by implantation of human neural stem cells on VEGF-releasing PLGA microparticles. Biomaterials 2012; 33(30): 7435-46.
[http://dx.doi.org/10.1016/j.biomaterials.2012.06.085] [PMID: 22818980]
[100]
Zong X, Wu S, Li F, et al. Transplantation of VEGF-mediated bone marrow mesenchymal stem cells promotes functional improvement in a rat acute cerebral infarction model. Brain Res 2017; 1676: 9-18.
[http://dx.doi.org/10.1016/j.brainres.2017.08.006] [PMID: 28823954]
[101]
Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 1991; 88(20): 9267-71.
[http://dx.doi.org/10.1073/pnas.88.20.9267] [PMID: 1924389]
[102]
Liu H, Honmou O, Harada K, et al. Neuroprotection by PlGF gene-modified human mesenchymal stem cells after cerebral ischaemia. Brain 2006; 129(Pt 10): 2734-45.
[http://dx.doi.org/10.1093/brain/awl207] [PMID: 16901914]
[103]
Licznerski P, Jonas EA. BDNF signaling: Harnessing stress to battle mood disorder. Proceedings of the National Academy of Sciences 201803645.
[http://dx.doi.org/10.1073/pnas.1803645115]
[104]
Zhang Y, Pardridge WM. Blood-brain barrier targeting of BDNF improves motor function in rats with middle cerebral artery occlusion. Brain Res 2006; 1111(1): 227-9.
[http://dx.doi.org/10.1016/j.brainres.2006.07.005] [PMID: 16884698]
[105]
Berger C, Schabitz W-R, Wolf M, Mueller H, Sommer C, Schwab S. Hypothermia and brain-derived neurotrophic factor reduce glutamate synergistically in acute stroke. Exp Neurol 2004; 185(2): 305-12.
[http://dx.doi.org/10.1016/j.expneurol.2003.10.008] [PMID: 14736512]
[106]
Schäbitz WR, Sommer C, Zoder W, Kiessling M, Schwaninger M, Schwab S. Intravenous brain-derived neurotrophic factor reduces infarct size and counterregulates Bax and Bcl-2 expression after temporary focal cerebral ischemia. Stroke 2000; 31(9): 2212-7.
[http://dx.doi.org/10.1161/01.STR.31.9.2212] [PMID: 10978054]
[107]
Zhang X, Zhou Y, Li H, et al. Intravenous administration of DPSCs and BDNF improves neurological performance in rats with focal cerebral ischemia. Int J Mol Med 2018; 41(6): 3185-94.
[http://dx.doi.org/10.3892/ijmm.2018.3517] [PMID: 29512704]
[108]
Cattaneo E, McKay R. Proliferation and differentiation of neuronal stem cells regulated by nerve growth factor. Nature 1990; 347(6295): 762-5.
[http://dx.doi.org/10.1038/347762a0] [PMID: 2172829]
[109]
Rosenthal A, Shelton DL, Walicke PA. Methods for treating osteoarthritis pain by administering a nerve growth factor antagonist and compositions containing the same Google Patents 2019.
[110]
Chang DS, Hsu E, Hottinger DG, Cohen SP. Anti-nerve growth factor in pain management: current evidence. J Pain Res 2016; 9: 373-83.
[PMID: 27354823]
[111]
Shimohama S, Ogawa N, Tamura Y, et al. Protective effect of nerve growth factor against glutamate-induced neurotoxicity in cultured cortical neurons. Brain Res 1993; 632(1-2): 296-302.
[http://dx.doi.org/10.1016/0006-8993(93)91164-N] [PMID: 7908599]
[112]
Cheng S, Ma M, Ma Y, Wang Z, Xu G, Liu X. Combination therapy with intranasal NGF and electroacupuncture enhanced cell proliferation and survival in rats after stroke. Neurol Res 2009; 31(7): 753-8.
[http://dx.doi.org/10.1179/174313209X382557] [PMID: 19061539]
[113]
Ding J, Cheng Y, Gao S, Chen J. Effects of nerve growth factor and Noggin-modified bone marrow stromal cells on stroke in rats. J Neurosci Res 2011; 89(2): 222-30.
[http://dx.doi.org/10.1002/jnr.22535] [PMID: 21162129]
[114]
Nakamura T, Nishizawa T, Hagiya M, et al. Molecular cloning and expression of human hepatocyte growth factor. Nature 1989; 342(6248): 440-3.
[http://dx.doi.org/10.1038/342440a0] [PMID: 2531289]
[115]
Matsumoto K, Nakamura T. Emerging multipotent aspects of hepatocyte growth factor. J Biochem 1996; 119(4): 591-600.
[http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021283] [PMID: 8743556]
[116]
Shimamura M, Sato N, Oshima K, et al. Novel therapeutic strategy to treat brain ischemia: overexpression of hepatocyte growth factor gene reduced ischemic injury without cerebral edema in rat model. Circulation 2004; 109(3): 424-31.
[http://dx.doi.org/10.1161/01.CIR.0000109496.82683.49] [PMID: 14707023]
[117]
Sowa K, Nito C, Nakajima M, et al. Impact of dental pulp stem cells overexpressing hepatocyte growth factor after cerebral ischemia/reperfusion in rats. Mol Ther Methods Clin Dev 2018; 10: 281-90.
[http://dx.doi.org/10.1016/j.omtm.2018.07.009] [PMID: 30151417]


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