Long-term neuroblast migration along blood vessels in an area with transient angiogenesis and increased vascularization after stroke
Abstract
Background and Purpose— Stroke induced by middle cerebral artery occlusion (MCAO) causes long-term formation of new striatal neurons from stem/progenitor cells in the subventricular zone (SVZ). We explored whether MCAO leads to hypoxia, changes in vessel density, and angiogenesis in the ipsilateral SVZ and adjacent striatum, and determined the relation between the migrating neuroblasts and the vasculature. Methods— Adult rats were subjected to 2 hours of MCAO. Hypoxia was studied by injecting Hypoxyprobe-1 during MCAO or 6 weeks later. Vessel density and length was estimated using stereology. New cells were labeled with 5′-bromo-2′deoxyuridine (BrdU) during weeks 1 and 2 or 7 and 8 after MCAO, and angiogenesis was assessed immunohistochemically with antibodies against BrdU and endothelial cell markers. Distance from neuroblasts to nearest vessel was measured using confocal microscopy. Results— The ischemic insult caused transient hypoxia and early, low-grade angiogenesis, but no damage or increase of vascular density in the SVZ. Angiogenesis was detected during the first 2 weeks in the dorsomedial striatum adjacent to the SVZ, which also showed long-lasting increase of vascularization. At 2, 6, and 16 weeks after MCAO, the majority of neuroblasts migrated through this area toward the damage, closely associated with blood vessels. Conclusions— The vasculature plays an important role for long-term striatal neurogenesis after stroke. During several months, neuroblasts migrate close to blood vessels through an area exhibiting early vascular remodeling and persistently increased vessel density. Optimizing vascularization should be an important strategy to promote neurogenesis and repair after stroke.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The finding that neural precursor cells prevent ischaemic injury and promote neurological recovery could be attributed to bystander effects from interaction of neuroblasts with microvasculature near the lesion, creating an environment that promotes brain remodelling.
“The finding that neural precursor cells prevent ischaemic injury and promote neurological recovery could be attributed to bystander effects related to the interaction of neuroblasts with the microvasculature in the vicinity of the ischaemic lesion, which creates an environment that promotes brain remodelling (figure 2).14,15,37,45”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [37]
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 [37]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The efficiency of systematic sampling in stereology and its prediction *
Gundersen, H., & Jensen, E. B. V. (1987) · Journal of Microscopy · doi:10.1111/j.1365-2818.1987.tb02837.x · Cited by 3,586 · see citing works
Neuronal replacement from endogenous precursors in the adult brain after stroke
Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., & Lindvall, O. (2002) · Nature Medicine · doi:10.1038/nm747 · Cited by 2,799 · see citing works
Self-citationEndothelial Cells Stimulate Self-Renewal and Expand Neurogenesis of Neural Stem Cells
Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N. E., Vincent, P. A., Pumiglia, K. M., & Temple, S. (2004) · Science · doi:10.1126/science.1095505 · Cited by 1,538 · see citing works
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia
Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X. O., Logvinova, A., & Greenberg, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200317977 · Cited by 1,189 · see citing works
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia
Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X. O., Logvinova, A. V., & Greenberg, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17977 · Cited by 1,181 · see citing works
Jin, K., Minami, M., Lan, J., Mao, X., Batteur, S., Simon, R., & Greenberg, D. A. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.081011098 · Cited by 1,117 · see citing works
Rat forebrain neurogenesis and striatal neuron replacement after focal stroke
Parent, J. M., Vexler, Z. S., Gong, C., Derugin, N., & Ferriero, D. M. (2002) · Annals of Neurology · doi:10.1002/ana.10393 · Cited by 1,020 · see citing works
Experimental studies of ischemic brain edema
Koizumi, J.-I., Yoshida, Y., Nakazawa, T., & Ooneda, G. (1986) · Nosotchu · doi:10.3995/jstroke.8.1 · Cited by 996 · see citing works
A Neurovascular Niche for Neurogenesis after Stroke
Ohab, J. J., Fleming, S., Blesch, A., & Carmichael, S. T. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4323-06.2006 · Cited by 878 · see citing works
Wang, L., Zhang, Z., Wang, Y., Zhang, R., & Chopp, M. (2004) · Stroke · doi:10.1161/01.str.0000132196.49028.a4 · Cited by 760 · see citing works
Coordinated Interaction of Neurogenesis and Angiogenesis in the Adult Songbird Brain
Louissaint, A., Rao, S., Leventhal, C., & Goldman, S. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00722-5 · Cited by 735 · see citing works
Yamashita, T., Ninomiya, M., Hernandez-Acosta, P., García‐Verdugo, J. M., Sunabori, T., Sakaguchi, M., Adachi, K., Kojima, T., Hirota, Y., Kawase, T., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0149-06.2006 · Cited by 720 · see citing works
Persistent Production of Neurons from Adult Brain Stem Cells During Recovery after Stroke
Thored, P., Arvidsson, A., Cacci, E., Ahlenius, H., Kallur, T., Darsalia, V., Ekdahl, C. T., Kokaia, Z., & Lindvall, O. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0281 · Cited by 714 · see citing works
Self-citationMarti, H. J. H., Bernaudin, M., Bellail, A., Schoch, H., Euler, M., Petit, E., & Risau, W. (2000) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64964-4 · Cited by 680 · see citing works
Zhang, R. L., Zhang, Z. G., Zhang, L., & Chopp, M. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00117-8 · Cited by 576 · see citing works
Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum
Jin, K., Sun, Y., Xie, L., Peel, A. L., Mao, X. O., Parmentier‐Batteur, S., & Greenberg, D. A. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00159-3 · Cited by 515 · see citing works
Vascular remodeling by intussusceptive angiogenesis
Djonov, V., Baum, O., & Burri, P. H. (2003) · Cell and Tissue Research · doi:10.1007/s00441-003-0784-3 · Cited by 327 · see citing works
Robin, A. M., Zhang, Z. G., Wang, L., Zhang, R. L., Katakowski, M., Zhang, L., Wang, Y., Zhang, C., & Chopp, M. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600172 · Cited by 303 · see citing works
Zhang, R., Zhang, Z., Zhang, C., Zhang, L., Robin, A., Wang, Y., Lu, M., & Chopp, M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1109-04.2004 · Cited by 205 · see citing works
Neonatal hypoxic?ischemic injury increases forebrain subventricular zone neurogenesis in the mouse
Plane, J. M., Liu, R., Wang, T., Silverstein, F. S., & Parent, J. M. (2004) · Neurobiology of Disease · doi:10.1016/j.nbd.2004.04.003 · Cited by 182 · see citing works
Spatial and temporal expression of short, long/medium, or both opsins in human fetal cones
Xiao, M., & Hendrickson, A. E. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001002)425:4 · Cited by 165 · see citing works
Hyperthermia complicates middle cerebral artery occlusion induced by an intraluminal filament
Zhao, Q., Memezawa, H., Smith, M., & Siejö, B. K. (1994) · Brain Research · doi:10.1016/0006-8993(94)91071-5 · Cited by 164 · see citing works
Yang, Z., & Levison, S. W. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.12.059 · Cited by 133 · see citing works
Larsen, Gundersen, & Nielsen (1998) · Journal of Microscopy · doi:10.1046/j.1365-2818.1998.00365.x · Cited by 126 · see citing works
Liu, X., Zhang, Z. G., Zhang, R. L., Gregg, S. R., Morris, D. C., Wang, Y., & Chopp, M. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600371 · Cited by 115 · see citing works
Kokaia, Z., Andsberg, G., Martı́nez-Serrano, A., & Lindvall, O. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00579-4 · Cited by 114 · see citing works
Self-citationNeurogenesis in the adult rat brain after intermittent hypoxia
Zhu, L., Zhao, T., Li, H.-S., Zhao, H., Wu, L., Ding, A.-S., Fan, W.-H., & Fan, M. (2005) · Brain Research · doi:10.1016/j.brainres.2005.04.075 · Cited by 100 · see citing works
Electroconvulsive seizures induce endothelial cell proliferation in adult rat hippocampus
Hellsten, J., Wennström, M., Bengzon, J., Mohapel, P., & Tingström, A. (2003) · Biological Psychiatry · doi:10.1016/j.biopsych.2003.08.013 · Cited by 97 · see citing works
Cerebral Ischemia and Angiogenesis
Hayashi, T., Deguchi, K., Nagotani, S., Zhang, H., Sehara, Y., Tsuchiya, A., & Abe, K. (2006) · Current Neurovascular Research · doi:10.2174/156720206776875902 · Cited by 88 · see citing works
Secretion of brain‐derived neurotrophic factor from brain microvascular endothelial cells
Wang, H., Ward, N., Boswell, M., & Katz, D. M. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04682.x · Cited by 81 · see citing works
Migration and fate of newly born cells after focal cortical ischemia in adult rats
Gotts, J. E., & Chesselet, M.-F. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20434 · Cited by 67 · see citing works
Vascular changes in the subventricular zone after distal cortical lesions
Gotts, J. E., & Chesselet, M. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.02.001 · Cited by 47 · see citing works
Mitogen-Activated Protein Kinase Signaling, Oxygen Sensors and Hypoxic Induction of Neurogenesis
Zhou, L., & Miller, C. A. (2006) · Neurodegenerative Diseases · doi:10.1159/000092093 · Cited by 17 · see citing works
Noto, T., Furuichi, Y., Ishiye, M., Matsuoka, N., Aramori, I., Mutoh, S., Yanagihara, T., & MANABE, N. (2006) · Journal of Veterinary Medical Science · doi:10.1292/jvms.68.803 · Cited by 15 · see citing works
Neurogenesis in the adult rat brain after intermittent hypoxia
Zhu, Z., Ll, Zhao, Li, HS, Wu, Ly, Ding, As, Fan, J., et al. (2006) · 中国生物学文摘 · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hip- pocampal neurogenesis. J Comp Neurol. 2000;425:479 -494.
Cited by
Sorted by citations
Ross, R., Blair, S. N., Arena, R., Church, T. S., Després, J.-P., Franklin, B. A., Haskell, W. L., Kaminsky, L. A., Levine, B. D., Lavie, C. J., et al. (2016) · Circulation · doi:10.1161/cir.0000000000000461 · Cited by 2,486 · see citing works
The Science of Stroke: Mechanisms in Search of Treatments
Moskowitz, M. A., Lo, E. H., & Iadecola, C. (2010) · Neuron · doi:10.1016/j.neuron.2010.07.002 · Cited by 1,930 · see citing works
Human Hippocampal Neurogenesis Persists throughout Aging
Boldrini, M., Fulmore, C. A., Tartt, A. N., Simeon, L. R., Pavlova, I., Poposka, V., Rosoklija, G. B., Stankov, A., Arango, V., Dwork, A. J., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.03.015 · Cited by 1,345 · see citing works
Neurogenesis and Exercise: Past and Future Directions
van Praag, H. (2008) · NeuroMolecular Medicine · doi:10.1007/s12017-008-8028-z · Cited by 645 · see citing works
Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic
Zhang, Z. G., & Chopp, M. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70061-4 · Cited by 596 · see citing works
Forebrain neurogenesis after focal Ischemic and traumatic brain injury
Kernie, S. G., & Parent, J. M. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.11.002 · Cited by 426 · see citing works
Vascular endothelial growth factor: a neurovascular target in neurological diseases
Lange, C. M., Storkebaum, E., de Almodóvar, C. R., Dewerchin, M. A., & Carmeliet, P. (2016) · Nature Reviews Neurology · doi:10.1038/nrneurol.2016.88 · Cited by 374 · see citing works
Thored, P., Heldmann, U., Gomes‐Leal, W., Gisler, R., Darsalia, V., Taneera, J., Nygren, J. M., Jacobsen, S. W., Ekdahl, C. T., Kokaia, Z., et al. (2009) · Glia · doi:10.1002/glia.20810 · Cited by 378 · see citing works
Self-citationAdult neurogenesis and the olfactory system
Whitman, M. C., & Greer, C. A. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.07.003 · Cited by 360 · see citing works
Boldrini, M., Hen, R., Underwood, M. D., Rosoklija, G. B., Dwork, A. J., Mann, J. J., & Arango, V. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.04.024 · Cited by 348 · see citing works
Hermann, D. M., & Chopp, M. (2012) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70039-x · Cited by 333 · see citing works
Neurogenesis and Inflammation after Ischemic Stroke: What is Known and Where We Go from Here
Tobin, M. K., Bonds, J. A., Minshall, R. D., Pelligrino, D. A., Testai, F. D., & Lazarov, O. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.130 · Cited by 327 · see citing works
Prakash, R., & Carmichael, S. T. (2015) · Current Opinion in Neurology · doi:10.1097/wco.0000000000000248 · Cited by 296 · see citing works
Kojima, T., Hirota, Y., Ema, M., Takahashi, S., Miyoshi, I., Okano, H., & Sawamoto, K. (2010) · Stem Cells · doi:10.1002/stem.306 · Cited by 307 · see citing works
Coupling of neurogenesis and angiogenesis after ischemic stroke
Ruan, L., Wang, B. Z., Zhuge, Q., & Jin, K. (2015) · Brain Research · doi:10.1016/j.brainres.2015.02.042 · Cited by 300 · see citing works
Angiogenesis, neurogenesis and brain recovery of function following injury.
Xiong, Y., Mahmood, A., & Chopp, M. (2010) · PubMed · Cited by 297 · see citing works
Ergul, A., Alhusban, A., & Fagan, S. C. (2012) · Stroke · doi:10.1161/strokeaha.111.642710 · Cited by 275 · see citing works
Neurogenesis following Stroke Affecting the Adult BrainPreprint
Lindvall, O., & Kokaia, Z. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a019034 · Cited by 242 · see citing works
Self-citationMartino, G., Pluchino, S., Bonfanti, L., & Schwartz, M. (2011) · Physiological Reviews · doi:10.1152/physrev.00032.2010 · Cited by 240 · see citing works
Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex
Arnò, B., Grassivaro, F., Rossi, C., Bergamaschi, A., Castiglioni, V., Furlan, R., Greter, M., Favaro, R., Comı, G., Becher, B., et al. (2014) · Nature Communications · doi:10.1038/ncomms6611 · Cited by 233 · see citing works
Cell migration in the normal and pathological postnatal mammalian brain
Cayre, M., Canoll, P., & Goldman, J. E. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.02.001 · Cited by 235 · see citing works
Neuronal regeneration in a zebrafish model of adult brain injury
Kishimoto, N., Shimizu, K., & Sawamoto, K. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.007336 · Cited by 220 · see citing works
Candelario‐Jalil, E. (2009) · PubMed · Cited by 219 · see citing works
New approaches for brain repair-from rescue to reprogramming
Barker, R. A., Götz, M., & Parmar, M. (2018) · Nature · doi:10.1038/s41586-018-0087-1 · Cited by 214 · see citing works
Neural stem cell therapies and hypoxic-ischemic brain injury
Huang, L., & Zhang, L. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.05.004 · Cited by 208 · see citing works
Neural stem cell therapy for subacute and chronic ischemic stroke
Boese, A. C., Le, Q.-S. E., Pham, D., Hamblin, M. H., & Lee, J.-P. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0913-2 · Cited by 205 · see citing works
Paczkowska, E., Kucia, M., Koziarska, D., Hałasa, M., Safranow, K., Masiuk, M., Karbicka, A., Nowik, M., Nowacki, P., Ratajczak, M. Z., et al. (2009) · Stroke · doi:10.1161/strokeaha.108.535062 · Cited by 201 · see citing works
Baumgart, E. V., Barbosa, J. S., Bally-Cuif, L., Götz, M., & Ninkovic, J. (2012) · Glia · doi:10.1002/glia.22269 · Cited by 193 · see citing works
Vascular Endothelial Growth Factor Increases Neurogenesis after Traumatic Brain Injury
Thau‐Zuchman, O., Shohami, E., Alexandrovich, A. G., & Leker, R. R. (2010) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.271 · Cited by 185 · see citing works
Blood vessels form a migratory scaffold in the rostral migratory stream
Whitman, M. C., Fan, W., Rela, L., Rodriguez‐Gil, D. J., & Greer, C. A. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22093 · Cited by 167 · see citing works
Ischemic stroke and neurogenesis in the subventricular zone
Zhang, R. L., Zhang, Z. G., & Chopp, M. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.05.027 · Cited by 158 · see citing works
Detante, O., Moisan, A., Dimastromatteo, J., Richard, M., Riou, L. M., Grillon, E., Barbier, E., Desruet, M.-D., de Fraipont, F., Segebarth, C. M., et al. (2009) · Cell Transplantation · doi:10.3727/096368909x474230 · Cited by 149 · see citing works
Christie, K. J., & Turnley, A. M. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2012.00070 · Cited by 146 · see citing works
Grade, 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
Houlton, J., Abumaria, N., Hinkley, S. F. R., & Clarkson, A. N. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00790 · Cited by 138 · see citing works
Ekstrand, J., Hellsten, J., & Tingström, A. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.06.085 · Cited by 139 · see citing works
Neurogenesis in the aging brain
Apple, D. M., Fonseca, R. S., & Kokovay, E. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.06.116 · Cited by 140 · see citing works
Saha, B., Péron, S., Murray, K., Jaber, M., & Gaillard, A. (2013) · Stem Cell Research · doi:10.1016/j.scr.2013.06.006 · Cited by 136 · 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
Zhao, L., & Willing, A. E. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.01.004 · Cited by 135 · see citing works
Chen, J., He, J., Ni, R., Yang, Q., Zhang, Y., & Luo, L. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.03.022 · Cited by 132 · see citing works
Cellular Mechanisms of Neurovascular Damage and Repair After Stroke
Arai, K., Lok, J. M., Guo, S., Hayakawa, K., Xing, C., & Lo, E. H. (2011) · Journal of Child Neurology · doi:10.1177/0883073811408610 · Cited by 125 · see citing works
Wang, J., Chen, S., Zhang, W., Chen, Y., & Bihl, J. C. (2020) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13455 · Cited by 127 · see citing works
Mine, Y., Tatarishvili, J., Oki, K., Monni, E., Kokaia, Z., & Lindvall, O. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.12.006 · Cited by 127 · see citing works
Self-citationZhang, R. L., Chopp, M., Gregg, S. R., Toh, Y., Roberts, C., LeTourneau, Y., Buller, B., Jia, L., Davarani, S. P. N., & Zhang, Z. G. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.55 · Cited by 120 · see citing works
“Neuroblasts generated in the SVZ migrate toward the ischemic boundary, and neuroblasts are closely associated with cerebral vessels (Zhang et al, 2004a; Yamashita et al, 2006; Thored et al, 2007).”
BackgroundNeuropathophysiology of Brain Injury
Quillinan, N., Herson, P. S., & Traystman, R. J. (2016) · Anesthesiology Clinics · doi:10.1016/j.anclin.2016.04.011 · Cited by 119 · see citing works
Zhang, L., Li, Y., Zhang, C., Chopp, M., Gosiewska, A., & Hong, K. (2011) · Stroke · doi:10.1161/strokeaha.110.593129 · Cited by 118 · see citing works
Diverse Roles of the Vasculature within the Neural Stem Cell Niche
Goldberg, J. S., & Hirschi, K. K. (2009) · Regenerative Medicine · doi:10.2217/rme.09.61 · Cited by 117 · see citing works
Are the neuroprotective effects of exercise training systemically mediated?
Tari, A. R., Norevik, C. S., Scrimgeour, N. R., Kobro‐Flatmoen, A., Storm‐Mathisen, J., Bergersen, L. H., Wrann, C. D., Selbæk, G., Kivipelto, M., Moreira, J. B. N., et al. (2019) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2019.02.003 · Cited by 120 · see citing works
Hansen, T. M., Moss, A., & Brindle, N. P. J. (2008) · Current Neurovascular Research · doi:10.2174/156720208786413433 · Cited by 115 · see citing works
Utility of Exosomes in Ischemic and Hemorrhagic Stroke Diagnosis and Treatment
Lee, E. C., Ha, T. W., Lee, D.-H., Hong, D.-Y., Park, S.-W., Lee, J. Y., Lee, M. R., & Oh, J. S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23158367 · Cited by 118 · see citing works
Paliouras, G. N., Hamilton, L. K., Aumont, A., Joppé, S. E., Barnabé‐Heider, F., & Fernandes, K. J. L. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2248-12.2012 · Cited by 113 · see citing works
Degeneration and repair in central nervous system disease
Lo, E. H. (2010) · Nature Medicine · doi:10.1038/nm.2226 · Cited by 109 · see citing works
Effects of Granulocyte-Colony Stimulating Factor After Stroke in Aged Rats
Popa‐Wagner, A., Stöcker, K., Bălşeanu, T. A., Rogalewski, A., Diederich, K., Minnerup, J., Mărgăritescu, C., & Schäbitz, W. (2010) · Stroke · doi:10.1161/strokeaha.109.575621 · Cited by 107 · see citing works
Berg, D. A., Kirkham, M., Beljajeva, A., Knapp, D., Habermann, B. H., Ryge, J., Tanaka, E. M., & Simon, A. (2010) · Development · doi:10.1242/dev.055541 · Cited by 106 · see citing works
Tepavčević, V., Lazarini, F., Alfaro‐Cervelló, C., Kerninon, C., Yoshikawa, K., García‐Verdugo, J. M., Lledo, P., Nait‐Oumesmar, B., & Evercooren, A. B. (2011) · Journal of Clinical Investigation · doi:10.1172/jci59145 · Cited by 106 · see citing works
Fessler, E. B., Chibane, F. L., Wang, Z., & Chuang, D. (2013) · Current Pharmaceutical Design · doi:10.2174/1381612811319280009 · Cited by 105 · see citing works
Therapeutic use of extracellular mitochondria in CNS injury and disease
Nakamura, Y., Park, J., & Hayakawa, K. (2019) · Experimental Neurology · doi:10.1016/j.expneurol.2019.113114 · Cited by 105 · see citing works
Crosstalk between cerebral endothelium and oligodendrocyte
Miyamoto, N., Pham, L. D., Seo, J. H., Kim, K., Lo, E. H., & Arai, K. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1488-9 · Cited by 103 · see citing works
Liu, X., Chopp, M., Zhang, R. L., Hozeska‐Solgot, A., Gregg, S. R., Buller, B., Lü, M., & Zhang, Z. G. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.006551 · Cited by 103 · see citing works
Increased subventricular zone-derived cortical neurogenesis after ischemic lesion
Kreuzberg, M. M., Kanov, E. V., Timofeev, O. N., Schwaninger, M., Monyer, H., & Khodosevich, K. V. (2010) · Experimental Neurology · doi:10.1016/j.expneurol.2010.08.006 · Cited by 101 · see citing works
Biphasic Mechanisms of Neurovascular Unit Injury and Protection in CNS Diseases
Maki, T., Hayakawa, K., Pham, L. D., Xing, C., Lo, E. H., & Arai, K. (2013) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527311312030004 · Cited by 101 · see citing works
Endothelial Progenitor Cells: Therapeutic Perspective for Ischemic Stroke
Zhao, Y., Yuan, B., Chen, J., Feng, D., Zhao, B., Qin, C., & Chen, Y. (2012) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12040 · Cited by 99 · see citing works
Cerebral Neovascularization in Diabetes: Implications for Stroke Recovery and beyond
Ergul, A., Abdelsaid, M. A., Fouda, A. Y., & Fagan, S. C. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.18 · Cited by 100 · see citing works
Sandvig, I., Augestad, I. L., Håberg, A. K., & Sandvig, A. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13959 · Cited by 94 · see citing works
New Vessels after Stroke: Postischemic Neovascularization and Regeneration
Liman, T., & Endres, M. (2012) · Cerebrovascular Diseases · doi:10.1159/000337155 · Cited by 97 · see citing works
Hutchings, G., Janowicz, K., Moncrieff, L., Dompé, C., Strauss, E., Kocherova, I., Nawrocki, M. J., Kruszyna, Ł., Wąsiatycz, G., Antosik, P., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113790 · Cited by 96 · see citing works
Oxygen, a Key Factor Regulating Cell Behavior during Neurogenesis and Cerebral Diseases
Zhang, K., Zhu, L., & Fan, M. (2011) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00005 · Cited by 96 · see citing works
Roitbak, T., Li, L., & Cunningham, L. A. (2008) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2008.38 · Cited by 94 · see citing works
Tseng, K.-Y., Anttila, J. E., Khodosevich, K. V., Tuominen, R. K., Lindahl, M., Domanskyi, A., & Airavaara, M. (2017) · Molecular Therapy · doi:10.1016/j.ymthe.2017.09.019 · Cited by 93 · see citing works
Guerra, M. M., Henzi, R., Ortloff, A., Lichtin, N., Vío, K., Jimenez, A. J., Domínguez-Pinos, D., González, C., Jara, M. C., Hinostroza, F., et al. (2015) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000203 · Cited by 94 · see citing works
Role of neural precursor cells in promoting repair following stroke
Dibajnia, P., & Morshead, C. M. (2012) · Acta Pharmacologica Sinica · doi:10.1038/aps.2012.107 · Cited by 93 · see citing works
Candelario, K. M., Shuttleworth, C. W., & Cunningham, L. A. (2013) · Journal of Neurochemistry · doi:10.1111/jnc.12204 · Cited by 92 · see citing works
Injury and repair in the neurovascular unit
Xing, C., Hayakawa, K., Lok, J. M., Arai, K., & Lo, E. H. (2012) · Neurological Research · doi:10.1179/1743132812y.0000000019 · Cited by 91 · see citing works
Chemokines direct neural progenitor cell migration following striatal cell loss
Gordon, R. J., McGregor, A. L., & Connor, B. J. (2009) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2009.03.001 · Cited by 90 · see citing works
Endothelial Progenitor Cell Research in Stroke
Rouhl, R. P. W., van Oostenbrugge, R. J., Damoiseaux, J. G. M. C., Tervaert, J.-W. C., & Lodder, J. (2008) · Stroke · doi:10.1161/strokeaha.107.507251 · Cited by 90 · see citing works
Wang, J., Su, Q., Lv, Q., Cai, B., Xiaohalati, X., Wang, G., Wang, Z., & Wang, L. (2021) · Nano Letters · doi:10.1021/acs.nanolett.1c00719 · Cited by 89 · see citing works
Astrocyte Signaling in the Neurovascular Unit After Central Nervous System Injury
Huang, L., Nakamura, Y., Lo, E. H., & Hayakawa, K. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020282 · Cited by 87 · see citing works
The early contribution of cerebrovascular factors to the pathogenesis of Alzheimer’s disease
Pimentel‐Coelho, P. M., & Rivest, S. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08126.x · 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
The role of the immune system in central nervous system plasticity after acute injury
Peruzzotti‐Jametti, L., Donegà, M., Giusto, E., Mallucci, G., Marchetti, B., & Pluchino, S. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.04.036 · Cited by 84 · see citing works
Li, Y., Chang, S., Li, W., Tang, G., Ma, Y., Liu, Y., Yuan, F., Zhang, Z., Yang, G., & Wang, Y. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0865-6 · Cited by 82 · see citing works
Regeneration of the ischemic brain by engineered stem cells: Fuelling endogenous repair processes
van Velthoven, C. T. J., Kavelaars, A., van Bel, F., & Heijnen, C. J. (2009) · Brain Research Reviews · doi:10.1016/j.brainresrev.2009.03.003 · Cited by 75 · see citing works
Neurogenesis in Neurodegenerative Diseases: Role of MFG-E8
Cheyuo, C., Aziz, M., & Wang, P. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00569 · Cited by 75 · see citing works
Dillen, Y., Kemps, H., Gervois, P., Wolfs, E., & Bronckaers, A. (2019) · Translational Stroke Research · doi:10.1007/s12975-019-00717-8 · Cited by 76 · see citing works
Schmidt, N. O., Koeder, D., Messing, M., Mueller, F.-J., Aboody, K. S., Kim, S. U., Black, P. M., Carroll, R. S., Westphal, M., & Lamszus, K. (2009) · Brain Research · doi:10.1016/j.brainres.2009.02.065 · Cited by 74 · see citing works
Mechanisms and Functional Significance of Stroke-Induced Neurogenesis
Marlier, Q., Verteneuil, S., Vandenbosch, R., & Malgrange, B. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00458 · Cited by 75 · see citing works
Abdelsaid, M. A., Prakash, R., Li, W., Coucha, M. M., Hafez, S. S., Johnson, M. H., Fagan, S. C., & Ergul, A. (2014) · Diabetes · doi:10.2337/db14-1423 · Cited by 72 · see citing works
Therapeutic application of exosomes in ischaemic stroke
Li, Y.-F., Tang, Y., & Yang, G. (2021) · Stroke and Vascular Neurology · doi:10.1136/svn-2020-000419 · Cited by 73 · see citing works
Simão, F., Pagnussat, A. S., Seo, J. H., Navaratna, D., Leung, W., Lok, J. M., Guo, S., Waeber, C., Salbego, C. G., & Lo, E. H. (2012) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2012.2 · Cited by 71 · see citing works
Wesley, U. V., Vemuganti, R., Ayvaci, E. R., & Dempsey, R. J. (2012) · Brain Research · doi:10.1016/j.brainres.2012.12.008 · Cited by 70 · see citing works
Enhanced neurogenesis and cell migration following focal ischemia and peripheral stimulation in mice
Li, W., Yu, S. P., Ogle, M. E., Ding, X. S., & Wei, L. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20674 · Cited by 69 · see citing works
Long-Term Stimulation of Neural Progenitor Cell Migration After Cortical Ischemia in Mice
Osman, A. M., Porritt, M. J., Nilsson, M., & Kuhn, H. G. (2011) · Stroke · doi:10.1161/strokeaha.111.627802 · Cited by 70 · see citing works
Hung, H., Wu, C., Chien, S., & Hsu, S. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2008.12.003 · Cited by 68 · see citing works
Home sweet home: the neural stem cell niche throughout development and after injury
Ruddy, R. M., & Morshead, C. M. (2017) · Cell and Tissue Research · doi:10.1007/s00441-017-2658-0 · Cited by 66 · see citing works
Hassani, Z., O’Reilly, J., Pearse, Y., Stroemer, P., Tang, E., Sinden, J. D., Price, J., & Thuret, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050444 · Cited by 67 · see citing works
Sun, F., Wang, X., Mao, X., Xie, L., & Jin, K. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046326 · Cited by 65 · see citing works
Roles for HIF-1α in neural stem cell function and the regenerative response to stroke
Cunningham, L. A., Candelario, K. M., & Li, L. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.08.002 · Cited by 66 · see citing works
- Authors
- Thored, P., Wood, J., Arvidsson, A., Cammenga, J., Kokaia, Z., & Lindvall, O.
- Affiliations
- From Laboratory of Neurogenesis and Cell Therapy (P.T., J.W., A.A., O.L.), Section of Restorative Neurology, Wallenberg Neuroscience Center, University Hospital, Lund, Sweden; Laboratory of Gene Therapy and Molecular Medicine (J.C.), Wallenberg Neuroscience Center, University Hospital, Lund, Sweden; Laboratory of Neural Stem Cell Biology (Z.K.), Section of Restorative Neurology, University Hospital, Lund, Sweden; Lund Strategic Research Center for Stem Cell Biology and Cell Therapy (P.T., J.W., A.A....
- Lund University (SE)
- Venue
- Stroke
- Published
- 2007-11
- Volume
- 38
- Issue
- 11
- Pages
- 3032-3039
- ISSN
- 0039-2499 (ISSN-L)
- 1524-4628
- OpenAlex
- W2134717451
- Cited by
- 421
- References
- 34
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 14 · 2023: 13 · 2022: 13 · 2021: 22 · 2020: 16 · 2019: 22 · 2018: 23 · 2017: 31 · 2016: 23 · 2015: 24 · 2014: 32 · 2013: 30 · 2012: 40
- FWCI
- 7.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Stroke (publishedVersion)
- PubMed (publishedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- Stiftelsen för Strategisk Forskning
- Vetenskapsrådet
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- neuroblast migration, angiogenesis, subventricular zone, striatal neurogenesis, middle cerebral artery occlusion, hypoxia, vascular remodeling, vessel density
- MeSH terms
- Animals, Cell Count, Cell Differentiation, Cell Movement, Cells, Cultured, Hypoxia, Brain, Cerebral Arteries, Corpus Striatum, Disease Models, Animal, Male, Nerve Regeneration, Neuronal Plasticity, Neurons, Stem Cells, Telencephalon, Time Factors, Rats, Wistar, Disease Progression, Neovascularization, Physiologic, Recovery of Function, Infarction, Middle Cerebral Artery, Stroke, Lateral Ventricles, Cell Proliferation, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review