Post-acute delivery of erythropoietin induces stroke recovery by promoting perilesional tissue remodelling and contralesional pyramidal tract plasticity
Open accessAbstract
The promotion of post-ischaemic motor recovery remains a major challenge in clinical neurology. Recently, plasticity-promoting effects have been described for the growth factor erythropoietin in animal models of neurodegenerative diseases. To elucidate erythropoietin's effects in the post-acute ischaemic brain, we examined how this growth factor influences functional neurological recovery, perilesional tissue remodelling and axonal sprouting of the corticorubral and corticobulbar tracts, when administered intra-cerebroventricularly starting 3 days after 30 min of middle cerebral artery occlusion. Erythropoietin administered at 10 IU/day (but not at 1 IU/day), increased grip strength of the contralesional paretic forelimb and improved motor coordination without influencing spontaneous locomotor activity and exploration behaviour. Neurological recovery by erythropoietin was associated with structural remodelling of ischaemic brain tissue, reflected by enhanced neuronal survival, increased angiogenesis and decreased reactive astrogliosis that resulted in reduced scar formation. Enhanced axonal sprouting from the ipsilesional pyramidal tract into the brainstem was observed in vehicle-treated ischaemic compared with non-ischaemic animals, as shown by injection of dextran amines into both motor cortices. Despite successful remodelling of the perilesional tissue, erythropoietin enhanced axonal sprouting of the contralesional, but not ipsilesional pyramidal tract at the level of the red and facial nuclei. Moreover, molecular biological and histochemical studies revealed broad anti-inflammatory effects of erythropoietin in both hemispheres together with expression changes of plasticity-related molecules that facilitated contralesional axonal growth. Our study establishes a plasticity-promoting effect of erythropoietin after stroke, indicating that erythropoietin acts via recruitment of contralesional rather than of ipsilesional pyramidal tract projections.
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Post-ischaemic endogenous plasticity partly compensates for loss of axons in target structures of damaged fibre bundles at various brain levels and spinal cord.
“Post-ischaemic endogenous plasticity partly compensates for the loss of axons in target structures of damaged fibre bundles at various levels of the brain (eg, red nucleus and facial nucleus) and spinal cord.12,19,24”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
Surviving pyramidal tract axons distal to the ischaemic injury sprout.
“Surviving pyramidal tract axons distal to the site of ischaemic injury sprout.19”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
Stroke induces anterograde Wallerian degeneration of pyramidal tract axons, with degree depending on severity of ischaemic insult.
“Stroke induces anterograde Wallerian degeneration of pyramidal tract axons, the degree of which depends on the severity of the ischaemic insult (figure 1).19,21,22”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
Neurorestorative treatments do not necessarily promote growth of terminal axons distal to injury, as shown after erythropoietin and VEGF.
“Importantly, neurorestorative treatments do not necessarily promote the growth of terminal axons distal to the site of injury, as was shown after delivery of the growth factors erythropoietin and vascular endothelial growth factor (VEGF).19,24”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
In rodents, beneficial effects of neurorestorative treatments were reported even when treatments were initiated days, weeks, or months after stroke.
“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 [19]
Terminal axonal sprouting is enhanced in both ipsilesional and contralesional pyramidal tract systems.
“Terminal axonal sprouting is enhanced in both the ipsilesional19,24 and the contra lesional12,19 pyramidal tract system.”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
This lesion-remote plasticity involves midline crossing of fibres from contralesional to ipsilesional hemisphere at the red nucleus and re-entry into contralesional hemicord at cervical spinal cord.
“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 [19]
Contralesional plasticity as a basis for neurological recovery occurs in several species, including rats, mice, and macaques.
“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 [19]
Axonal growth responses are relatively uniform across different treatment types, with contralesional sprouting evident after growth factors, anti-NogoA antibodies, neurostimulants, and cell-based therapeutics.
“Importantly, axonal growth responses are relatively uniform for different types of treatment: contralesional sprouting was evident after delivery of growth factors,19,24 neutralising antibodies directed against the axonal growth inhibitor NogoA,11,17 neurostimulants (eg, amphetamine), 29 and cell-based therapeutics, namely bone-marrow-derived stromal cells12,30 or neural pre cursor cells.15”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
Contralesional sprouting after growth factor treatment is associated with profound alterations of gene expression, including downregulation of axonal growth inhibitors and inflammatory signals near the contralesional pyramidal tract.
“Contralesional sprouting after treatment with growth factors is associated with profound alterations of gene expression, including the downregulation of axonal growth inhibitors19,24 and inflammatory signals19,31 in the vicinity of the contralesional pyramidal tract.”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [19]
Homologous fibres from the contralesional motor cortex grow across the midline to reach denervated neurons in target structures of the lesioned pyramidal tract.
“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 [19]
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Self-citation
- Authors
- Reitmeir, R., Kilic, E., Kilic, Ü., Bacigaluppi, M., ElAli, A., Salani, G., Pluchino, S., Gassmann, M., & Hermann, D. M.
- Affiliations
- Essen University Hospital (DE)
- IRCCS Ospedale San Raffaele (IT)
- University of Zurich (CH)
- Venue
- Brain
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-12-22
- Volume
- 134
- Issue
- 1
- Pages
- 84-99
- ISSN
- 0006-8950 (ISSN-L)
- 1460-2156
- OpenAlex
- W2151922165
- Cited by
- 156
- References
- 55
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 7 · 2023: 8 · 2022: 17 · 2021: 9 · 2020: 9 · 2019: 13 · 2018: 11 · 2017: 13 · 2016: 12 · 2015: 8 · 2014: 16 · 2013: 7 · 2012: 13
- FWCI
- 9.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Brain (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- reroDoc Digital Library (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Yale University
- Universität Zürich
- Topics
- Health Sciences › Medicine › Rehabilitation › Stroke Rehabilitation and Recovery
- Health Sciences › Medicine › Hematology › Erythropoietin and Anemia Treatment
- Life Sciences › Neuroscience › Neurology › Neurological Disorders and Treatments
- Keywords
- erythropoietin, stroke recovery, motor recovery, corticobulbar tract, middle cerebral artery occlusion, angiogenesis, reactive astrogliosis, anti-inflammatory activity, red nucleus, facial nucleus, brainstem projections, neuroplasticity
- MeSH terms
- Analysis of Variance, Animals, Brain, Brain Ischemia, Erythropoietin, Exploratory Behavior, Immunohistochemistry, Male, Motor Activity, Neuronal Plasticity, Neurons, Blotting, Western, Hand Strength, Recovery of Function, Reverse Transcriptase Polymerase Chain Reaction, Stroke, Rotarod Performance Test, Mice
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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 ›
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