Patterns and dynamics of subventricular zone neuroblast migration in the ischemic striatum of the adult mouse
Open accessAbstract
The migratory behavior of neuroblasts after a stroke is poorly understood. Using time-lapse microscopy, we imaged migration of neuroblasts and cerebral vessels in living brain slices of adult doublecortin (DCX, a marker of neuroblasts) enhanced green fluorescent protein (eGFP) transgenic mice that were subjected to 7 days of stroke. Our results show that neuroblasts originating in the subventricular zone (SVZ) of adult mouse brain laterally migrated in chains or individually to reach the ischemic striatum. The chains were initially formed at the border between the SVZ and the striatum by neuroblasts in the SVZ and then extended to the striatum. The average speed of DCX-eGFP-expressing cells within chains was 28.67 ± 1.04 μm/h, which was significantly faster ( P < 0.01) than the speed of the cells in the SVZ (17.98 ± 0.57 μm/h). Within the ischemic striatum, individual neuroblasts actively extended or retracted their processes, suggestive of probing the immediate microenvironment. The neuroblasts close to cerebral blood vessels exhibited multiple processes. Our data suggest that neuroblasts actively interact with the microenvironment to reach the ischemic striatum by multiple migratory routes.
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After stroke, neural precursor cells proliferate and migrate toward the ischaemic lesion, propagating in chains along blood vessels.
“When a stroke occurs, these cells proliferate and migrate in the direction of the ischaemic lesion, propagating in chains along blood vessels.37,38”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [38]
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Cites
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“…Boundary On the basis of immunohistochemistry, with an antibody against DCX in fixed brain tissue, we and others have shown that stroke increases neuroblasts in the ischemic SVZ and the ischemic boundary (Zhang et al, 2001, 2004a; Arvidsson et al, 2002; Parent et al, 2002; Jin et al, 2003).”
BackgroundMethodSelf-citationDirected migration of neuronal precursors into the ischemic cerebral cortex and striatum
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“…Boundary On the basis of immunohistochemistry, with an antibody against DCX in fixed brain tissue, we and others have shown that stroke increases neuroblasts in the ischemic SVZ and the ischemic boundary (Zhang et al, 2001, 2004a; Arvidsson et al, 2002; Parent et al, 2002; Jin et al, 2003).”
BackgroundResultInfluentialThree‐dimensional reconstruction of the antennal lobe in Drosophila melanogaster
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BackgroundDirect Evidence for Homotypic, Glia-Independent Neuronal Migration
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BackgroundA rat model of focal embolic cerebral ischemia
Zhang, R. L., Chopp, M., Zhang, Z. G., Jiang, Q., & Ewing, J. R. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00580-5 · Cited by 332 · cited 4× · see citing works
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MethodInfluentialSelf-citationWang, L., Zhang, Z. G., Zhang, R. L., Gregg, S. R., Hozeska-Solgot, A., LeTourneau, Y., Wang, Y., & Chopp, M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.5380-05.2006 · Cited by 316 · cited 3× · see citing works
“These molecules likely act as extrinsic factors generated by the ischemic lesion to attract neuroblasts to the ischemic lesion (Lee et al, 2006; Ohab et al, 2006; Robin et al, 2006; Wang et al, 2006; Teng et al, 2008).”
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“These molecules likely act as extrinsic factors generated by the ischemic lesion to attract neuroblasts to the ischemic lesion (Lee et al, 2006; Ohab et al, 2006; Robin et al, 2006; Wang et al, 2006; Teng et al, 2008).”
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“These molecules likely act as extrinsic factors generated by the ischemic lesion to attract neuroblasts to the ischemic lesion (Lee et al, 2006; Ohab et al, 2006; Robin et al, 2006; Wang et al, 2006; Teng et al, 2008).”
BackgroundTeng, H., Zhang, Z. G., Wang, L., Zhang, R. L., Zhang, L., Morris, D., Gregg, S. R., Wu, Z., Jiang, A., Lu, M., et al. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600573 · Cited by 254 · cited 3× · see citing works
“These molecules likely act as extrinsic factors generated by the ischemic lesion to attract neuroblasts to the ischemic lesion (Lee et al, 2006; Ohab et al, 2006; Robin et al, 2006; Wang et al, 2006; Teng et al, 2008).”
BackgroundSelf-citationSuzuki, S. O., & Goldman, J. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-04240.2003 · Cited by 237 · cited 5× · see citing works
“However, after stroke, many neuroblasts emigrated laterally from the SVZ to reach the ischemic striatum by either chains or individual migration, suggesting that neuroblasts cross some structural and/molecular barriers between the SVZ and the adjacent striatum that constrains neuroblast migration under physiologic con…”
BackgroundResultInfluentialKoizumi, H., Higginbotham, H., Poon, T., Tanaka, T., Brinkman, B. C., & Gleeson, J. G. (2006) · Nature Neuroscience · doi:10.1038/nn1704 · Cited by 237 · cited 1× · see citing works
“In addition to a marker of migrating neuroblasts, DCX plays an essential role in maintaining bipolar morphology of neuroblasts (Koizumi et al, 2006; Ocbina et al, 2006; Friocourt et al, 2007; Walker et al, 2007).”
BackgroundBlood Vessels Form a Scaffold for Neuroblast Migration in the Adult Olfactory Bulb
Bovetti, S., Hsieh, Y.-C., Bovolin, P., Perroteau, I., Toida, K., & Puché, A. C. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0678-07.2007 · Cited by 227 · cited 4× · see citing works
“…(RMS), as chains through tunnels formed by astrocytes or use blood vessels as a scaffold, to the olfactory bulb where they differentiate into granule and periglomerular neurons throughout the adult life (Doetsch et al, 1997; Luskin et al, 1997; Garcia-Verdugo et al, 1998; Bovetti et al, 2007).”
BackgroundInfluentialKirschenbaum, B., Doetsch, F. K., Lois, C., & Álvarez-Buylla, A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-06-02171.1999 · Cited by 224 · cited 1× · see citing works
“…also observed in brain saggital sections including the striatal SVZ (Supplementary Figure 2), suggesting that the chain migration of DCX-eGFP-expressing cells to the ischemic striatum is unlikely caused by interrupting the RMS after coronal sectioning (Alonso et al, 1999; Kirschenbaum et al, 1999).”
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“…(RMS), as chains through tunnels formed by astrocytes or use blood vessels as a scaffold, to the olfactory bulb where they differentiate into granule and periglomerular neurons throughout the adult life (Doetsch et al, 1997; Luskin et al, 1997; Garcia-Verdugo et al, 1998; Bovetti et al, 2007).”
BackgroundDorsal Radial Glia Generate Olfactory Bulb Interneurons in the Postnatal Murine Brain
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“Neuroblasts in the SVZ are a heterogeneous population derived from different neural stem cells (Willaime-Morawek et al, 2006; Merkle et al, 2007; Ventura and Goldman, 2007; Young et al, 2007).”
BackgroundBoth Doublecortin and Doublecortin-Like Kinase Play a Role in Cortical Interneuron Migration
Friocourt, G., Liu, J. S.-H., Antypa, M., Rakić, S., Walsh, C. A., & Parnavelas, J. G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4530-06.2007 · Cited by 147 · cited 1× · see citing works
“In addition to a marker of migrating neuroblasts, DCX plays an essential role in maintaining bipolar morphology of neuroblasts (Koizumi et al, 2006; Ocbina et al, 2006; Friocourt et al, 2007; Walker et al, 2007).”
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“Neuroblasts express doublecortin (DCX), a protein that regulates neuroblast migration (Yang et al, 2004; Nam et al, 2007; Walker et al, 2007).”
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“Consistent with earlier findings, under nonischemic conditions, neuroblasts migrated dorsa-ventrally within the SVZ of the lateral ventricle and never crossed the SVZ striatum border (Suzuki and Goldman, 2003; Nam et al, 2007; Zhang et al, 2007).”
BackgroundMethodResultInfluentialSelf-citationDistribution of doublecortin expressing cells near the lateral ventricles in the adult mouse brain
Yang, H. K. C., Sundholm‐Peters, N. L., Goings, G. E., Walker, A. S., Hyland, K. V., & Szele, F. G. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20071 · Cited by 118 · cited 1× · see citing works
“Neuroblasts express doublecortin (DCX), a protein that regulates neuroblast migration (Yang et al, 2004; Nam et al, 2007; Walker et al, 2007).”
BackgroundDynamic features of postnatal subventricular zone cell motility: A two‐photon time‐lapse study
Nam, S. C., Kim, Y., Dryanovski, D. I., Walker, A. S., Goings, G. E., Woolfrey, K. M., Kang, S. S., Chu, C., Chenn, A., Erdélyi, F., et al. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21473 · Cited by 111 · cited 4× · see citing works
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BackgroundResultInfluentialA Mouse Model of Embolic Focal Cerebral Ischemia
Zhang, Z., Chopp, M., Zhang, R. L., & Goussev, A. V. (1997) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199710000-00010 · Cited by 101 · see citing works
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“Histologic analysis of fixed brain specimens suggests that stroke redirects neuroblasts in the SVZ to the ischemic striatum (Arvidsson et al, 2002; Parent et al, 2002; Jin et al, 2003; Zhang et al, 2003, 2004a).”
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Doe, C. Q., Fuerstenberg, S., & Peng, C. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199808)36:2 · Cited by 85 · see citing works
Embryonic cortical neural stem cells migrate ventrally and persist as postnatal striatal stem cells
Willaime‐Morawek, S., Seaberg, R. M., Batista, C. M. C., Labbé, E., Attisano, L., Gorski, J. A., Jones, K. R., Kam, A., Morshead, C. M., & van der Kooy, D. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200604123 · Cited by 73 · cited 1× · see citing works
“Neuroblasts in the SVZ are a heterogeneous population derived from different neural stem cells (Willaime-Morawek et al, 2006; Merkle et al, 2007; Ventura and Goldman, 2007; Young et al, 2007).”
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“Interestingly, using two-photon microscopy, Zhao and Nam (2007) show that an average speed of nestin-GFPexpressing cells in the RMS is 30 mm/h measured by three-dimensional calculation in 3-week-old nestinGFP mice, which is comparable with an average speed of 29 mm/h observed in DCX-eGFP-expressing cells within a chai…”
BackgroundMethodSelf-citationDoublecortin is necessary for the migration of adult subventricular zone cells from neurospheres
Ocbina, P. J. R., Dizon, M. L. V., Shin, L., & Szele, F. G. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2006.06.014 · Cited by 51 · cited 1× · see citing works
“In addition to a marker of migrating neuroblasts, DCX plays an essential role in maintaining bipolar morphology of neuroblasts (Koizumi et al, 2006; Ocbina et al, 2006; Friocourt et al, 2007; Walker et al, 2007).”
BackgroundVisualization of cell cycling by an improvement in slice culture methods
Miyata, T., Kawaguchi, A., Saito, K., Kuramochi, H., & Ogawa, M. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10335 · Cited by 31 · cited 2× · see citing works
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MethodLiu, X., Chopp, M., Zhang, X. G., Zhang, R. L., Buller, B., Hozeska‐Solgot, A., Gregg, S. R., & Zhang, Z. G. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.119 · Cited by 24 · cited 1× · see citing works
“Stroke induces changes in gene profiles of neuroblasts localized to the SVZ (Liu et al, 2009).”
BackgroundSelf-citationZhao, L., & Nam, S. C. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.07.032 · Cited by 18 · cited 3× · see citing works
“Journal of Cerebral Blood Flow & Metabolism (2009) 29, 1240–1250 & 2009 ISCBFM All rights reserved 0271-678X/09 $32.00 www.jcbfm.com nestin-positive cells in the olfactory bulb under normal and ischemic conditions (Nam et al, 2007; Zhao and Nam, 2007).”
BackgroundMethodInfluential
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Hermann, D. M., & Chopp, M. (2012) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70039-x · Cited by 333 · see citing works
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Exosomes Derived from Mesenchymal Stromal Cells Promote Axonal Growth of Cortical Neurons
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Neurogenesis following Stroke Affecting the Adult BrainPreprint
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“Neuroblasts in the migrating chains were highly motile and extended or retracted their processes (Zhang et al. 2009).”
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Self-citationExosomes in stroke pathogenesis and therapy
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“57 μm/h out of SVZ following ischemia (Zhang et al., 2009).”
BackgroundThe MicroRNA-17–92 Cluster Enhances Axonal Outgrowth in Embryonic Cortical Neurons
Zhang, Y., Ueno, Y., Liu, X., Buller, B., Wang, X., Chopp, M., & Zhang, Z. G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5180-12.2013 · Cited by 161 · see citing works
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MethodInfluentialSelf-citationMechanisms of neuronal migration in the adult brain
Kaneko, N., Sawada, M., & Sawamoto, K. (2017) · Journal of Neurochemistry · doi:10.1111/jnc.14002 · Cited by 150 · see citing works
Oligodendrogenesis after cerebral ischemia
Zhang, R., Chopp, M., & Zhang, Z. G. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00201 · Cited by 149 · see citing works
““fncel-07-00201” — 2013/10/27 — 17:51 — page 1 — #1 REVIEW ARTICLE published: 29 October 2013 doi: 10.3389/fncel.2013.00201 Oligodendrogenesis after cerebral ischemia”
BackgroundInfluentialSelf-citationGrade, S., Weng, Y. C., Snapyan, M., Križ, J., Malva, J. O., & Saghatelyan, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055039 · Cited by 143 · see citing works
Stem cell transplantation therapy for multifaceted therapeutic benefits after stroke
Wei, L., Wei, Z. Z., Jiang, M. Q., Mohamad, O., & Yu, S. P. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.03.003 · Cited by 143 · see citing works
The Role of SDF-1/CXCR4/CXCR7 in Neuronal Regeneration after Cerebral Ischemia
Cheng, X., Wang, H., Zhang, X., Zhao, S., Zhou, Z., Mu, X., Zhao, C., & Teng, W. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00590 · Cited by 138 · see citing works
“In addition, stroke-induced angiogenesis has been shown to enhance poststroke neurogenesis (Jin et al., 2006; Thored et al., 2007) (Zhang et al., 2009).”
Backgroundβ1 integrin signaling promotes neuronal migration along vascular scaffolds in the post-stroke brain
Fujioka, T., Kaneko, N., Ajioka, I., Nakaguchi, K., Omata, T., Ohba, H., Fässler, R., García‐Verdugo, J. M., Sekiguchi, K., Matsukawa, N., et al. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.01.005 · Cited by 110 · see citing works
“, 2009) and in post-stroke striatum toward the injured area (Kojima et al., 2010; Ohab et al., 2006; Yamashita et al., 2006; Zhang et al., 2009).”
BackgroundBernstock, J. D., Peruzzotti‐Jametti, L., Ye, D. G., Gessler, F. A., Maric, D., Vicario, N., Lee, Y.-J., Pluchino, S., & Hallenbeck, J. M. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x17700432 · Cited by 99 · see citing works
“pathotropism) may integrate into the ischemic tissue.(19,20) Beyond the replacement of damaged cells, extensive stem cell graft-to-host communication after NSC transplantation in experimental stroke leads to significant trophic/plasticity effects and beneficial immunomodulatory actions.”
BackgroundStroke Increases Neural Stem Cells and Angiogenesis in the Neurogenic Niche of the Adult Mouse
Zhang, R. L., Chopp, M., Roberts, C. J., Liu, X., Wei, M., Nejad‐Davarani, S. P., Wang, X., & Zhang, Z. G. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113972 · Cited by 98 · see citing works
“These findings are consistent with published studies [11, 13, 14, 25].”
BackgroundResultInfluentialSelf-citationLim, T. C., Toh, W. S., Wang, L., Kurisawa, M., & Spector, M. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.01.037 · Cited by 94 · see citing works
“rostral migratory stream towards the olfactory bulb) and instead, home towards brain injury sites [3,42,43].”
BackgroundKaneko, N., Herranz‐Pérez, V., Otsuka, T., Sano, H., Ohno, N., Omata, T., Nguyen, H. B., Thai, T. Q., Nambu, A., Kawaguchi, Y., et al. (2018) · Science Advances · doi:10.1126/sciadv.aav0618 · Cited by 85 · see citing works
Hermann, D. M., Peruzzotti‐Jametti, L., Schlechter, J., Bernstock, J. D., Doeppner, T. R., & Pluchino, S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00291 · Cited by 84 · see citing works
Opportunities and Challenges: Stem Cell‐Based Therapy for the Treatment of Ischemic Stroke
Tang, Y., Ma, Y., Zhang, Z., Wang, Y., & Yang, G. (2015) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12386 · Cited by 77 · see citing works
“After ischemic stroke onset, endogenous NSCs could proliferate and migrate into the injured region, promoting tissue repair [15,16].”
BackgroundSelf-citationDillen, Y., Kemps, H., Gervois, P., Wolfs, E., & Bronckaers, A. (2019) · Translational Stroke Research · doi:10.1007/s12975-019-00717-8 · Cited by 75 · see citing works
Basal ganglia function, stuttering, sequencing and repair in adult songbirds
Kubíková, Ľ., Bosíková, E., Cviková, M., Lukacova, K., Scharff, C., & Jarvis, E. D. (2014) · Scientific Reports · doi:10.1038/srep06590 · Cited by 74 · see citing works
An Overview of Adult Neurogenesis
Ribeiro, F. F., & Xapelli, S. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-74046-7_7 · Cited by 72 · see citing works
MicroRNAs in Cerebral Ischemia-Induced Neurogenesis
Liu, X., Chopp, M., Zhang, R. L., & Zhang, Z. G. (2013) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31829e4963 · Cited by 71 · see citing works
Self-citationVenkat, P., Chen, J., & Chopp, M. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x18782789 · Cited by 71 · see citing works
Self-citationZhang, Y., Xiong, Y., Mahmood, A., Meng, Y., Qu, C., Schallert, T. J., & Chopp, M. (2009) · Brain Research · doi:10.1016/j.brainres.2009.07.077 · Cited by 70 · see citing works
“…percentage of newborn neurons found in the injured cortex, suggesting that neuroblasts may migrate from the SVZ into the injured cortex, where some of the SVZ-derived neuroblasts differentiate into mature neurons (Goings et al., 2004; Sundholm-Peters et al., 2005; Zhang et al., 2004, 2008, 2009).”
BackgroundSelf-citationStem cells and stroke: opportunities, challenges and strategies
Burns, T. C., & Steinberg, G. K. (2011) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2011.552883 · Cited by 67 · see citing works
“SDF-1 and angiopoietin redirect neuroblasts from the SVZ and RMS along blood vessels toward the infarct region [80].”
BackgroundCiticoline Enhances Neuroregenerative Processes After Experimental Stroke in Rats
Diederich, K., Frauenknecht, K. B. M., Minnerup, J., Schneider, B. K., Schmidt, A., Altach, E., Eggert, V., Sommer, C., & Schäbitz, W. (2012) · Stroke · doi:10.1161/strokeaha.112.654806 · Cited by 68 · see citing works
Function of neural stem cells in ischemic brain repair processes
Zhang, R., Zhang, Z., & Chopp, M. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16674487 · Cited by 67 · see citing works
Self-citationMagueresse, C. L., Alfonso, J., Bark, C., Eliava, M., Khrulev, S., & Monyer, H. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr302 · Cited by 66 · see citing works
“Neuroblasts en route to the poststroke area were found in close proximity to blood vessels (Yamashita et al. 2006; Zhang et al. 2009).”
BackgroundStromal cell-derived factor-1 and its receptor CXCR4 in adult neurogenesis after cerebral ischemia
Cui, L., Qu, H., Xiao, T., Zhao, M., Jolkkonen, J., & Zhao, C. (2013) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-120271 · Cited by 61 · see citing works
“Interestingly, neural progenitor cells are found in the vicinity of blood vessels in both intact or injured human or rodent brains (Jin et al., 2006; Palmer et al., 2000; Thored et al., 2007; Zhang et al., 2009), suggesting that blood vessels may be associated with the migration of cells after stroke.”
BackgroundInfluentialLim, T. C., Rokkappanavar, S., Toh, W. S., Wang, L., Kurisawa, M., & Spector, M. (2012) · The FASEB Journal · doi:10.1096/fj.12-221515 · Cited by 60 · see citing works
“S2) where cells were known to follow preceding cells (20) or use one another as guiding structures (7).”
BackgroundCofilin as a Promising Therapeutic Target for Ischemic and Hemorrhagic Stroke
Alhadidi, Q., Sayeed, M. S. B., & Shah, Z. A. (2015) · Translational Stroke Research · doi:10.1007/s12975-015-0438-2 · Cited by 57 · see citing works
Zhang, W., Wang, H., Zhang, H., Leak, R. K., Shi, Y., Hu, X., Gao, Y., & Chen, J. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.03.005 · Cited by 57 · see citing works
“Neurogenesis can occur in response to cerebral ischemia and is characterized by themigration of SVZ-derived neural precursor cells along the blood vessels to the site of ischemic lesion (Ruan et al., 2014; Zhang et al., 2009).”
Vascular regulation of adult neurogenesis under physiological and pathological conditions
Sawada, M., Matsumoto, M., & Sawamoto, K. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00053 · Cited by 57 · see citing works
“, 2006) and second, they migrate along blood vessels (Zhang et al., 2009; Kojima et al., 2010; Saha et al., 2013).”
BackgroundNeural Stem Cell Plasticity: Advantages in Therapy for the Injured Central Nervous System
Ottoboni, L., Merlini, A., & Martino, G. (2017) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2017.00052 · Cited by 55 · see citing works
“In stroke, transplanted NSCs directly modulate neuronal circuit plasticity (Zhang et al., 2009) through the expression of developmental molecules such as guidance molecules (i.e., slit, thrombospondin-1 and -2) and trophic factor such as VEGF (Andres et al., 2011).”
BackgroundAdult neurogenesis and its role in brain injury and psychiatric diseases
Hayashi, Y., Jinnou, H., Sawamoto, K., & Hitoshi, S. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14557 · Cited by 55 · see citing works
Cellular and Molecular Determinants of Stroke-Induced Changes in Subventricular Zone Cell Migration
Young, C. C., Brooks, K. J., Buchan, A. M., & Szele, F. G. (2010) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3435 · Cited by 55 · see citing works
“Time-lapse microscopy of acute slices after focal ischemia suggests that some of the Dcxþ neuroblasts made contacts with blood vessels during active migration, both in the early phase as the neuroblasts exit the SVZ, as well as in the striatum (53, 134).”
Young, C. C., van der Harg, J. M., Lewis, N. J., Brooks, K. J., Buchan, A. M., & Szele, F. G. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs049 · Cited by 52 · see citing works
“In support of this, timelapse imaging indicates that neuroblasts increase migratory speed as they exit the SVZ and enter the striatum post stroke (Zhang et al. 2009).”
Combination of Stem Cells and Rehabilitation Therapies for Ischemic Stroke
Berlet, R., Anthony, S., Brooks, B., Wang, Z.-J., Sadanandan, N., Shear, A., Cozene, B., Gonzales‐Portillo, B., Parsons, B., Salazar, F. E., et al. (2021) · Biomolecules · doi:10.3390/biom11091316 · Cited by 51 · see citing works
Magnusson, J. P., & Frisén, J. (2016) · Development · doi:10.1242/dev.133975 · Cited by 46 · see citing works
“The nearby subventricular zone was long thought to be the only source of adult-born striatal neurons, based on the fact that neuroblasts can migrate into the striatum after stroke (Li et al., 2010; Zhang et al., 2009).”
BackgroundA possible new focus for stroke treatment – migrating stem cells
Sullivan, R., Duncan, K., Dailey, T., Kaneko, Y., Tajiri, N., & Borlongan, C. V. (2015) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2015.1043264 · Cited by 44 · see citing works
“Chemokine signals such as SDF-1 (discussed above), VEGF, and angiopoietin are released from the ischemic tissue to influence the course of NSCs along blood vessels to reach the site of injury [38-41].”
BackgroundStem Cell Transplantation for Neuroprotection in Stroke
Shinozuka, K., Dailey, T., Tajiri, N., Ishikawa, H., Kaneko, Y., & Borlongan, C. V. (2013) · Brain Sciences · doi:10.3390/brainsci3010239 · Cited by 41 · see citing works
“Chemokine signals such as stromal-derived factor-1 (SDF-1), vascular endothelial growth factor (VEGF), and angiopoietin are released from ischemic tissue, influencing the course of the SVZ NSCs toward a path along blood vessels to reach the infarcted area [82–85].”
BackgroundEndogenous neurogenesis following ischaemic brain injury: Insights for therapeutic strategies
Merson, T. D., & Bourne, J. A. (2014) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2014.08.003 · Cited by 42 · see citing works
A vascular perspective on neuronal migration
Segarra, M., Kirchmaier, B. C., & Acker‐Palmer, A. (2015) · Mechanisms of Development · doi:10.1016/j.mod.2015.07.004 · Cited by 41 · see citing works
“Live imaging of cultured brain slices after ischemic injury displayed that SVZ-derived NPCs first extended their leading processes to blood vessels and migrated towards them (Kojima et al., 2010; Zhang et al., 2009).”
Luzzati, F., Marchis, S. D., Parlato, R., Gribaudo, S., Schütz, G., Fasolo, A., & Peretto, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025088 · Cited by 40 · see citing works
“In contrast to our results in CBCM mice, in vitro slice cultures of the striatum shortly after acute ischemic injury, showed that SVZ neuroblasts enter the striatum from the whole periventricular SVZ, often organized as chains [40,41].”
ResultAjioka, I., Jinnou, H., Okada, K., Sawada, M., Saitoh, S., & Sawamoto, K. (2014) · Tissue Engineering Part A · doi:10.1089/ten.tea.2014.0080 · Cited by 39 · see citing works
Liang, Y., Li, K., Riecken, K., Maslyukov, A., Gómez‐Nicola, D., Kovalchuk, Y., Fehse, B., & Garaschuk, O. (2016) · Cell Research · doi:10.1038/cr.2016.55 · Cited by 37 · see citing works
Regulation of adult neural precursor cell migration
Leong, S. Y., & Turnley, A. M. (2011) · Neurochemistry International · doi:10.1016/j.neuint.2010.12.024 · Cited by 37 · see citing works
Zhang, Y., Chopp, M., Liu, X., Kassis, H., Wang, X., Li, C., An, G., & Zhang, Z. G. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22292 · Cited by 35 · see citing works
“The distal axons of the cortical neurons stained with immunocytochemistry were imaged under a 403 objective using a laser-scanning confocal microscope (Zeiss LSM 510 NLO, Carl Zeiss, Germany) (Zhang et al., 2009).”
MethodSelf-citationNew Neurons in the Post-ischemic and Injured Brain: Migrating or Resident?
Nemirovich-Danchenko, N. M., & Khodanovich, M. Y. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00588 · Cited by 36 · see citing works
Sanberg, P. R., Eve, D. J., Metcalf, C., & Borlongan, C. V. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59544-7.00006-8 · Cited by 35 · see citing works
Wu, C., Wang, L., Su, Y.-T., Wei, W., & Tsai, K. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.09.014 · Cited by 34 · see citing works
Addington, C. P., Roussas, A., Dutta, D., & Stabenfeldt, S. E. (2015) · Biomarker Insights · doi:10.4137/bmi.s20062 · Cited by 33 · see citing works
Zhang, Y., Li, C., Qin, Y., Cepparulo, P., Millman, M., Chopp, M., Kemper, A., Szalad, A., Lu, X., Wang, L., et al. (2021) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12073 · Cited by 33 · see citing works
“The immunoreactive samples were imaged under a 63x objective by means of a laser-scanning confocal microscope (Zeiss LSM 510 NLO, Carl Zeiss, Germany) (Zhang et al., 2009, 2013).”
MethodSelf-citationEmerging scaffold- and cellular-based strategies for brain tissue regeneration and imaging
Collins, M. N., Zamboni, F., Serafin, A., Escobar, A., Stepanian, R., Culebras, M., Reis, R. L., & Oliveira, J. M. (2022) · In vitro models · doi:10.1007/s44164-022-00013-0 · Cited by 33 · see citing works
De-routing neuronal precursors in the adult brain to sites of injury: Role of the vasculature
Massouh, M., & Saghatelyan, A. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.12.021 · Cited by 32 · see citing works
“…labeling (Arvids-son et al., 2002; Parent et al., 2002b; Zhang et al., 2004a), DiI labeling (Jin et al., 2003), Cre-loxP reporter system (Yamashita et al., 2006), grafted cells in the SVZ (Zhang et al., 2003) and ex vivo imaging technique in the striatum of Dcx-eGFP mice (Zhang et al., 2009).”
InfluentialNeural Stem Cells and Ischemic Brain
Zhang, Z., & Chopp, M. (2016) · Journal of Stroke · doi:10.5853/jos.2016.00206 · Cited by 32 · see citing works
“In addition to the V/SVZ niche, increased neuroblasts induced by stroke in the V/SVZ migrate along cerebral blood vessels to peri-infarct regions where angiogenesis occurs.(36-40) Soluble molecules and their receptors mediate vascular-coupled neuroblast migration in ischemic brain, such as angiopoietin-1 (Ang1)/Tie2,…”
BackgroundSelf-citationZhang, W., Lin, H., Wen, Y., Su, L., Li, Y., & Luo, X. (2023) · Brain and Behavior · doi:10.1002/brb3.2912 · Cited by 32 · see citing works
“Moreover, studies report that postischemic angiogenesis follows a temporal course (Bi et al., 2022; Zhang et al., 2009).”
BackgroundThe use of bioactive matrices in regenerative therapies for traumatic brain injury
Tan, H. X., Borgo, M. P. D., Aguilar, M., Forsythe, J. S., Taylor, J. M., & Crack, P. J. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.11.032 · Cited by 32 · see citing works
Tissue Engineering and Biomaterial Strategies to Elicit Endogenous Neuronal Replacement in the Brain
Purvis, E. M., O’Donnell, J. C., Chen, H.-C. I., & Cullen, D. K. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00344 · Cited by 31 · see citing works
An Update on Translating Stem Cell Therapy for Stroke from Bench to Bedside
Dailey, T., Metcalf, C., Mosley, Y. I., Sullivan, R., Shinozuka, K., Tajiri, N., Pabon, M. M., Acosta, S., Kaneko, Y., van Loveren, H., et al. (2013) · Journal of Clinical Medicine · doi:10.3390/jcm2040220 · Cited by 31 · see citing works
“vessels to reach the infarcted area [85–88].”
The Effects of Extrinsic and Intrinsic Factors on Neurogenesis
Jiang, M. H., Jang, S. E., & Zeng, L. (2023) · Cells · doi:10.3390/cells12091285 · Cited by 31 · see citing works
“For example, after brain injury neuroblasts migrate individually, but a similar chain of neuroblasts migrating toward injured areas forms [56].”
BackgroundAdult neurogenesis from reprogrammed astrocytes
Griffiths, B. B., Bhutani, A., & Stary, C. M. (2019) · Neural Regeneration Research · doi:10.4103/1673-5374.270292 · Cited by 30 · see citing works
“Let-7b is highly expressed in both differentiated neurons and astrocytes and regulates proliferation and differentiation (Zhao et al., 2010). miR-9 helps drive neural stem cells toward a neural fate (Zhao et al., 2009).”
BackgroundStoll, E. A. (2014) · Molecular and Cellular Therapies · doi:10.1186/2052-8426-2-12 · Cited by 28 · see citing works
Khodanovich, M. Y., Gubskiy, I. L., Kudabaeva, M., Namestnikova, D. D., Kisel, A. A., Anan’ina, T. V., Tumentceva, Y. A., Mustafina, L. R., & Yarnykh, V. L. (2021) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x211020860 · Cited by 23 · see citing works
“Remodeling of damaged neural networks may lead to formation of new synaptic contacts and de novo axonal growth and myelination.(17,18) Therefore, accurate quantification of myelination is crucial for monitoring and predicting the effect of rehabilitation and neurorestorative therapies in stroke.”
BackgroundSalvianolic acid B alleviates neurological injury by upregulating stanniocalcin 1 expression
Bi, S., Dong, X.-Y., Wang, Z.-Y., Fu, S., Li, C., Wang, Z., Xie, F., Chen, X., Xu, H., Cai, X.-J., et al. (2022) · Annals of Translational Medicine · doi:10.21037/atm-21-4779 · Cited by 23 · see citing works
“However, previous studies reported that post-ischemic angiogenesis follows a temporal course (33).”
Maturation-dependent response of neurogenesis after traumatic brain injury in children.
Taylor, S. R., Smith, C. M., Harris, B. T., Costine, B. A., & Duhaime, A. (2013) · Journal of Neurosurgery: Pediatrics · doi:10.3171/2013.8.peds13154 · Cited by 26 · see citing works
Duncan, K., Gonzales-Portillo, G. S., Acosta, S. A., Kaneko, Y., Borlongan, C. V., & Tajiri, N. (2015) · Brain Research · doi:10.1016/j.brainres.2015.03.007 · Cited by 21 · see citing works
“NPCs have demonstrated the ability to travel from the SVZ to the post-ischemic striatum in MCAO rat models [27, 28].”
BackgroundPostnatal neuronal migration in health and disease
Nakajima, C., Sawada, M., & Sawamoto, K. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.06.001 · Cited by 21 · see citing works
Vascular damage in the central nervous system: a multifaceted role for vascular-derived TGF-β
Beck, K., & Schachtrup, K. (2011) · Cell and Tissue Research · doi:10.1007/s00441-011-1228-0 · Cited by 20 · see citing works
“In the damaged brain, NSCs appear in the vicinity of blood vessels near the injured area (Ohab et al. 2006; Thored et al. 2007; Zhang et al. 2009) and blood vessels play an important role as a scaffold for NSC migration towards the damaged brain area (Kojima et al. 2010).”
Regeneration using endogenous neural stem cells following neonatal brain injury
Jinnou, H. (2020) · Pediatrics International · doi:10.1111/ped.14368 · Cited by 20 · see citing works
Neuroplasticity and behavioral effects of fluoxetine after experimental stroke
Sun, Y., Sun, X., Qu, H., Zhao, S., Xiao, T., & Zhao, C. (2017) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-170725 · Cited by 19 · see citing works
“In addition, many neuroblasts are found in the vicinity of blood vessels in both intact and injured human or rodent brains, suggesting that blood vessels may be associated with the migration of cells after a stroke (Thored et al., 2007; Zhang et al., 2009).”
Noh, J., Oh, S., Lee, S., Lee, S., Kim, Y. H., Park, H.-J., Ju, J. H., Kim, H. S., Huh, J. Y., & Song, J. (2020) · Cell Proliferation · doi:10.1111/cpr.12884 · Cited by 21 · see citing works
ILC2 instructs neural stem and progenitor cells to potentiate neurorepair after stroke
Liu, G., Huang, H., Wang, Y., Han, Y., Wang, J., Shi, M., Zhou, P., Chen, C., Yu, Y., Liu, Q., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.03.014 · Cited by 18 · see citing works
Monitoring Brain Repair in Stroke Using Advanced Magnetic Resonance Imaging
Sztriha, L., Tuura, R., Modo, M., Barker, G. J., Williams, S., & Kalra, L. (2012) · Stroke · doi:10.1161/strokeaha.111.649244 · Cited by 17 · see citing works
Migratory Response of Cells in Neurogenic Niches to Neuronal Death: The Onset of Harmonic Repair?
Geribaldi‐Doldán, N., Carrascal, L., Pérez-García, P., Oliva, J. M., Pardillo-Díaz, R., Domínguez‐García, S., Utrera, C. B., Gómez‐Oliva, R., Martínez‐Ortega, S., Verástegui, C., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076587 · Cited by 15 · see citing works
“In the case of trauma and stroke, neuroblasts are able to migrate toward the injured site not only in chains but also individually, following bidirectional movements [58].”
BackgroundPromoting Neurological Recovery in the Post-Acute Stroke Phase: Benefits and Challenges
Hermann, D. M., & Chopp, M. (2014) · European Neurology · doi:10.1159/000365171 · Cited by 14 · see citing works
Self-citationMoon, Y., Kim, J. Y., Kim, W. R., Kim, H. J., Jang, M. J., Nam, Y., Kim, K., Kim, H., & Sun, W. (2013) · Stem Cells · doi:10.1002/stem.1420 · Cited by 14 · see citing works
“Induction of ERM phosphorylation by SDF1-CXCR4 signaling after injury Brain ischemia promotes regenerative responses, including the recruitment of endogenous neural progenitor cells to the damaged regions [3, 11, 49-51].”
BackgroundReview: Could neurotransmitters influence neurogenesis and neurorepair after stroke?
Sánchez-Mendoza, E. H., Bellver‐Landete, V., Merino, J. J., González, M. P., Martínez‐Murillo, R., & Oset‐Gasque, M. J. (2013) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12082 · Cited by 14 · see citing works
Geng, R., Wang, Y., Wang, R., Wu, J., & Bao, X. (2025) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00879 · Cited by 15 · see citing works
“The migrating CDX + progenitor cells move along the vascular system and aggregate, with ~ 35% of them localizing within a 5-μm range of the vessels (Zhang et al., 2009; Boese et al., 2018).”
Neuronal Migration in the Adult Brain
Sawada, M., Huang, S.-H., Hirota, Y., Kaneko, N., & Sawamoto, K. (2011) · Springer eBooks · doi:10.1007/978-4-431-53933-9_14 · Cited by 13 · see citing works
Tajiri, N., & Crowley, M. (2017) · Brain Circulation · doi:10.4103/bc.bc_17_17 · Cited by 13 · see citing works
“[21] In rat stroke models, NPCs have been observed to migrate from the SVZ to the postischemic infarct within the striatum.[25,26] The”
BackgroundLukacova, K., Pavukova, E., Košťál, Ľ., Bilčı́k, B., & Kubíková, Ľ. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.06.032 · Cited by 10 · see citing works
“…of striatal injury, the damage leads to increased cell proliferation in the rat SVZ (Zhang et al., 2001, 2004; Arvidsson et al., 2002; Darsalia et al., 2005) and the newly formed neuroblasts migrate into the damaged striatum (Arvidsson et al., 2002; Zhang et al., 2004, 2009; Kokaia et al., 2006).”
CXCL12-Mediated Murine Neural Progenitor Cell Movement Requires PI3Kβ Activation
Holgado, B., Martínez‐Muñoz, L., Sánchez‐Alcañiz, J. A., Lucas, P., Pérez-García, V., Pérez, G., Rodrı́guez-Frade, J. M., Nieto, M., Marín, Ó., Carrasco, Y. R., et al. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8451-5 · Cited by 9 · see citing works
Bernstock, J. D., Verheyen, J., Huang, B. Y., Hallenbeck, J. M., & Pluchino, S. (2014) · InTech eBooks · doi:10.5772/58599 · Cited by 8 · see citing works
“The neural precursors that develop, transmigrate and integrate display an innate form of pathotropism [229, 230].”
BackgroundLa thérapie cellulaire de l’accident vasculaire cérébral ischémique : du mythe à la réalité
Pellegrini, L., Bennis, Y., Guillet, B. A., Velly, L. J., Bruder, N. J., & Pisano, P. S. (2012) · Revue Neurologique · doi:10.1016/j.neurol.2012.08.009 · Cited by 8 · see citing works
The Emerging Impact of microRNAs in Neurotrauma Pathophysiology and Therapy
Bhalala, O. G. (2015) · Europe PMC (PubMed Central) · Cited by 8 · see citing works
Neural Stem Cells in Stroke: Intracerebral Approaches
Manley, N. C., Azevedo-Pereira, R. L., Bliss, T. M., & Steinberg, G. K. (2015) · Springer eBooks · doi:10.1007/978-3-319-15063-5_7 · Cited by 7 · see citing works
Adult neurogenesis and brain remodelling after brain injury: From bench to bedside?
Quintard, H., Heurteaux, C., & Ichaï, C. (2015) · Anaesthesia Critical Care & Pain Medicine · doi:10.1016/j.accpm.2015.02.008 · Cited by 6 · see citing works
Loss of LRP1 in Adult Neural Stem Cells Impairs Migration to Ischemic Lesions
Dietert, K., Mahesula, S., Hegde, S., Verschelde, J., Reed, P., Sprague, S. M., Kokovay, E., & Sayre, N. L. (2023) · Stem Cells · doi:10.1093/stmcls/sxad034 · Cited by 6 · see citing works
Cell therapy for ischemic stroke. Stem cell types and results of pre-clinical trials
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“Zhang et al [46] mostraron, además, que las CPN penetran en el estriado usando un patrón exploratorio en el que una de ellas emite proyeccioFigura 3.”
BackgroundDifferent Sources of Stem Cells for Transplantation Therapy in Stroke
Dailey, T., Eve, D. J., Tajiri, N., Lau, T., Mosley, Y. I., van Loveren, H., Sanberg, P. R., Kaneko, Y., & Borlongan, C. V. (2012) · Springer eBooks · doi:10.1007/978-3-7091-1175-8_3 · Cited by 3 · see citing works
Neuronal migration in the postnatal brain
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Compensatory Neurogenesis in the Injured Adult Brain
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“SVZ progenitor cells have also been observed to migrate in chains into the ischemic striatum and cortex (Arvidsson , et al. , 2002, Parent , et al. , 2002, Jin , et al. , 2003, Ohab , et al. , 2006, Yamashita , et al. , 2006, Zhang , et al. , 2009).”
Mechanisms of Plasticity Remodeling and Recovery
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Self-citation
- Authors
- Zhang, R. L., Chopp, M., Gregg, S. R., Toh, Y., Roberts, C., LeTourneau, Y., Buller, B., Jia, L., Davarani, S. P. N., & Zhang, Z. G.
- Affiliations
- Henry Ford Health (US)
- Department of Neurology, Henry Ford Health Sciences Center, Detroit, Michigan, USA
- Corresponding author
- Zhang, Zheng G
- Venue
- Journal of Cerebral Blood Flow & Metabolism
- Publisher
- SAGE Publications
- Published
- 2009-05-13
- Volume
- 29
- Issue
- 7
- Pages
- 1240-1250
- ISSN
- 0271-678X (ISSN-L)
- 1559-7016
- PMC
- PMC2741163
- OpenAlex
- W2027022086
- Cited by
- 120
- References
- 48
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 1 · 2023: 6 · 2022: 3 · 2021: 5 · 2020: 6 · 2019: 5 · 2018: 9 · 2017: 10 · 2016: 9 · 2015: 15 · 2014: 12 · 2013: 11 · 2012: 11
- FWCI
- 2.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Heart, Lung, and Blood Institute (R01HL064766, R01HL64766)
- National Institute of Neurological Disorders and Stroke (P50 NS23392, P01NS42345, P50NS023393, P01NS042345)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Keywords
- subventricular zone, neuroblast migration, stroke, doublecortin, lateral migration, migration speed, cerebral vasculature, microenvironment, adult neurogenesis, time-lapse microscopy
- MeSH terms
- Doublecortin Protein, Animals, Cell Movement, Brain Ischemia, Cerebral Ventricles, Cerebrovascular Circulation, Corpus Striatum, Kinetics, Neurons, Stem Cells, Microscopy, Video, Stroke, Mice
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