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Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain
Open accessAbstract
Stem cell transplantation promises new hope for the treatment of stroke although significant questions remain about how the grafted cells elicit their effects. One hypothesis is that transplanted stem cells enhance endogenous repair mechanisms activated after cerebral ischaemia. Recognizing that bilateral reorganization of surviving circuits is associated with recovery after stroke, we investigated the ability of transplanted human neural progenitor cells to enhance this structural plasticity. Our results show the first evidence that human neural progenitor cell treatment can significantly increase dendritic plasticity in both the ipsi- and contralesional cortex and this coincides with stem cell-induced functional recovery. Moreover, stem cell-grafted rats demonstrated increased corticocortical, corticostriatal, corticothalamic and corticospinal axonal rewiring from the contralesional side; with the transcallosal and corticospinal axonal sprouting correlating with functional recovery. Furthermore, we demonstrate that axonal transport, which is critical for both proper axonal function and axonal sprouting, is inhibited by stroke and that this is rescued by the stem cell treatment, thus identifying another novel potential mechanism of action of transplanted cells. Finally, we established in vitro co-culture assays in which these stem cells mimicked the effects observed in vivo. Through immunodepletion studies, we identified vascular endothelial growth factor, thrombospondins 1 and 2, and slit as mediators partially responsible for stem cell-induced effects on dendritic sprouting, axonal plasticity and axonal transport in vitro. Thus, we postulate that human neural progenitor cells aid recovery after stroke through secretion of factors that enhance brain repair and plasticity.
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In the citing paper
“With simple growth factor withdrawal for three weeks, most of these iPS-NPCs develop into neurons expressing Tuj1 or MAP250”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [50]
Experimental — accuracy not yet measuredIn the citing paper
“In rodents, beneficial effects were reported even when treatments were initiated days, weeks, or months after stroke.14–20”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“By contrast with neuroprotection, which requires an acute intervention, treatments promoting neurological recovery by remodelling of brain tissue can be instituted during the stroke recovery phase.10–15”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“By sharp contrast with neuroprotection, the efficacy of neuro restorative therapies does not depend on the successful reperfusion of ischaemic brain tissue.11,12,15,17,21”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“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 [15]
In the citing paper
“Meanwhile, evidence that neuro genesis contributes to functional neurological recovery has been obtained in studies with transgenic ablation of neural precursor cells expressing the marker doublecortin43 and in studies with exogenous delivery of adult neural precursor cells,14,15,44 which reported impaired or enhanced neurological recovery, respectively.”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“Instead, homologous fibres originating from the contralesional motor cortex grow out across the midline to reach denervated neurons in target structures of the lesioned pyramidal tract (figure 1).10–12,15,17,19,24”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“Contralesional plasticity as a basis for neurological recovery occurs in several species (eg, in rats,11,15,17 mice,12,19,24 and macaques32).”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“This lesion-remote plasticity involves the midline crossing of fibres from the contralesional to the ipsilesional hemisphere at the level of the red nucleus10,17,19,24 and the re-entry of fibres into the contralesional hemicord at the level of the cervical spinal cord (figure 1).11,12,15”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
In the citing paper
“Microvessels and neuroblasts mutually support each other via release of trophic factors, resulting in a tight interplay that stimulates brain remodelling processes, reducing delayed neuronal degeneration,14,45 promoting neuronal plasticity,15 modulating glial responses,14,46 and attenuating brain inflammation14,46 (figure 2).”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [15]
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Metadata
- Authors
- Andres, R. H., Horie, N., Slikker, W., Keren-Gill, H., Zhan, K., Sun, G., Manley, N. C., Pereira, M. P., Sheikh, L. A., McMillan, E. L., Schaar, B. T., Svendsen, C. N., Bliss, T. M., & Steinberg, G. K.
- Affiliations
- Stanford Medicine (US)
- Stanford University (US)
- University of Wisconsin–Madison (US)
- Cedars-Sinai Medical Center (US)
- Corresponding author
- Bliss, Tonya M.
- Steinberg, Gary K.
- ORCID
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2011-05-24
- Volume
- 134
- Issue
- 6
- Pages
- 1777-1789
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- PMC
- PMC3102243
- OpenAlex
- W2009703235
- Cited by
- 329
- References
- 71
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 18 · 2023: 18 · 2022: 14 · 2021: 22 · 2020: 20 · 2019: 16 · 2018: 23 · 2017: 30 · 2016: 18 · 2015: 39 · 2014: 28 · 2013: 33 · 2012: 24
- FWCI
- 10.19
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Brain (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Bern Open Repository and Information System (University of Bern) (submittedVersion, other-oa)
- Open Access CRIS of the University of Bern
- Funders
- National Science Foundation
- Hearst Foundations
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (123221, 117034, PASMP3-123221/1)
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01 NS27292, R01NS058784, P01 NS 37520, P01NS057778, P01NS037520, R01NS027292)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Keywords
- neural stem cell transplantation, neural progenitor cells, stroke, cerebral ischemia, structural plasticity, dendritic sprouting, axonal transport, corticospinal axons, functional recovery, vascular endothelial growth factor, thrombospondin, slits, co-culture, brain repair
- MeSH terms
- Analysis of Variance, Animals, Axonal Transport, Biotin, Cell Survival, Cells, Cultured, Cerebral Cortex, Brain Ischemia, Corpus Callosum, Dendrites, Dextrans, Disease Models, Animal, Fetus, Gene Expression Regulation, Humans, Male, Nerve Tissue Proteins, Neuronal Plasticity, Psychomotor Performance, Rats, Nude, RNA, Messenger, Time Factors, Vibrissae, Rats, Sprague-Dawley, Brain Infarction, Rats, Neural Stem Cells
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