An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke
Open accessAbstract
Stroke is an age-related disease. Recovery after stroke is associated with axonal sprouting in cortex adjacent to the infarct. The molecular program that induces a mature cortical neuron to sprout a new connection after stroke is not known. We selectively isolated neurons that sprout a new connection in cortex after stroke and compared their whole-genome expression profile to that of adjacent, non-sprouting neurons. This 'sprouting transcriptome' identified a neuronal growth program that consists of growth factor, cell adhesion, axonal guidance and cytoskeletal modifying molecules that differed by age and time point. Gain and loss of function in three distinct functional classes showed new roles for these proteins in epigenetic regulation of axonal sprouting, growth factor-dependent survival of neurons and, in the aged mouse, paradoxical upregulation of myelin and ephrin receptors in sprouting neurons. This neuronal growth program may provide new therapeutic targets and suggest mechanisms for age-related differences in functional recovery.
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In rodent and primate models of stroke, axonal sprouting and the formation of new connections occurs in motor, somatosensory and premotor areas.
“In rodent and primate models of stroke, axonal sprouting and the formation of new connections occurs in motor, somatosensory and premotor areas1–4.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results section (“ATRX mediates axonal sprouting after stroke”; page unavailable) reports stroke-induced sprouting in motor, premotor and somatosensory areas in mice. The paper also describes new projection patterns in rats, but the passages in our copy do not establish the claim for primate stroke models. (LLM, conf=0.88)
Experimental — accuracy not yet measuredGDF10 is one of the most highly upregulated genes during the initiation of axonal sprouting in peri-infarct cortical neurons in the aged brain.
“Within the post-stroke axonal sprouting transcriptome, Growth and Differentiation Factor 10 (GDF10) is one of the most highly upregulated genes during the initiation of axonal sprouting in peri-infarct cortical neurons in the aged brain.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results section reports that Gdf10 was upregulated in aged sprouting neurons at day 7 after stroke, and localizes GDF10 to peri-infarct cortical neurons. It does not identify Gdf10 as one of the most highly upregulated genes; it names Igf1 and osteopontin as the most differentially regulated genes. (LLM, conf=0.87)
Experimental — accuracy not yet measuredStroke induces axonal sprouting and the formation of new connections in peri-infarct cortex that link premotor, motor, somatosensory and association areas.
“Stroke induces axonal sprouting and the formation of new connections in peri-infarct cortex that link premotor, motor, somatosensory and association areas1–4.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results section (“ATRX mediates axonal sprouting after stroke”; page unavailable) reports increased peri-infarct connections and stroke-induced sprouting in motor, premotor and somatosensory areas. The paper also describes new connection patterns, but our copy does not establish the claim’s additional link to association areas. (LLM, conf=0.86)
Experimental — accuracy not yet measuredGDF10 is induced in sprouting neurons from aged rats during the initiation phase of axonal sprouting, 7 days after stroke, 1.32× with microarray and 3× with confirmatory qPCR (p<0.0009).
“GDF10 is induced in sprouting neurons from aged rats during the initiation phase of axonal sprouting, 7 days after stroke3: 1.32× with microarray and 3× with confirmatory qPCR (p<0.0009) at 7d after stroke3.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results sections on gene expression and mRNA confirmation report that day 7 was examined as an early stage of sprouting and that Gdf10 was upregulated in aged rat sprouting neurons in both the microarray and confirmatory qRT-PCR analyses. The passages in our copy do not give the claimed 1.32× and 3× changes or p<0.0009, so those numerical details remain unsupported. (LLM, conf=0.86)
Experimental — accuracy not yet measuredNucleotide-modified siRNA delivered directly into the infarct core produces protein knockdown over at least 2 weeks after stroke with GDF10.
“As previously shown in other gene systems3,4, nucleotide-modified siRNA delivered directly into the infarct core produces protein knockdown over at least 2 weeks after stroke with GDF10 (Supplementary Fig. 3a).”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results section, “ATRX mediates axonal sprouting after stroke” (page unavailable), reports ATRX knockdown in vivo after stroke using Atrx siRNA. Our copy does not establish that the siRNA was nucleotide-modified or delivered directly into the infarct core, or that protein knockdown lasted at least two weeks. It reports GDF10 expression after stroke, not GDF10 knockdown. (LLM, conf=0.82)
Experimental — accuracy not yet measured
GDF10 gain and loss of function was produced directly from the stroke through sustained release via biopolymer hydrogel, which produces release over 2-3 weeks from the stroke site without altering local inflammation, gliosis, neuronal or vascular structure.
“To test this hypothesis, GDF10 gain and loss of function was produced directly from the stroke through sustained release via biopolymer hydrogel, which produces release over 2–3 weeks from the stroke site3,4,28 without altering local inflammation, gliosis, neuronal or vascular structure4.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredStroke normally produces a limited pattern of axonal sprouting from motor or somatosensory cortex posteriorly to areas adjacent to or caudal to the stroke.
“Stroke normally produces a limited pattern of axonal sprouting from motor or somatosensory cortex posteriorly to areas adjacent to or caudal to the stroke2–4,28,29.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results section (“ATRX mediates axonal sprouting after stroke”; page unavailable) reports that stroke normally induces axonal sprouting in motor and somatosensory areas of peri-infarct cortex. The Discussion (“Growth factor dependence, epigenetic modifiers and growth inhibitors after stroke”; page unavailable) says this occurs locally and up to several millimeters from the infarct, but does not establish a specifically posterior or caudal direction or describe the pattern as limited. (LLM, conf=0.85)
Experimental — accuracy not yet measuredAfter stroke, axonal sprouting has been demonstrated in mice, rats and non-human primates.
“After stroke, axonal sprouting has been demonstrated in mice, rats and non-human primates1–4,10,38.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results sections on sprouting neurons and ATRX report post-stroke axonal sprouting in rats and mice. The cited paper does not report or identify a demonstration in non-human primates. Page numbers were not provided in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe biopolymer hydrogel releases both small and large molecules over a 3 week period from the infarct core.
“This biopolymer hydrogel releases both small and large molecules over a 3 week period from the infarct core3,4,29.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
The Results section (“IGF1 maintains cortical neurons after stroke”; page unavailable) reports sustained local release of IGF1 from a biopolymer hydrogel in the infarct cavity over four weeks. It does not establish release of both small and large molecules, and it gives four weeks rather than the claimed three-week period. (LLM, conf=0.86)
Experimental — accuracy not yet measuredStroke alone modestly but significantly induces axonal sprouting in the motor cortex adjacent to the stroke site compared to normal motor system connections.
“As reported previously3,4,28,29, stroke alone modestly but significantly induces axonal sprouting in the motor cortex adjacent to the stroke site compared to normal motor system connections (Supplementary Fig. 6b).”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
This experimental design has been validated by other groups conducting similar behavioral or tissue outcomes experiments.
“This experimental design has been validated by other groups conducting similar behavioral4 or tissue outcomes experiments3,4,28,29.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
Sample size for in vivo quantitative cortical mapping studies was estimated from previous publications with similar mechanistic studies.
“Animal number in in vivo quantitative cortical mapping studies utilizes spatial correlation statistics, so sample size was estimated from previous publications with similar mechanistic studies3,4,28,29.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [3]
Spatial orientation and distribution of fibres are controlled by Lingo1 and Nogo receptor 1, which direct newly formed axons to cortical areas otherwise not targeted.
“The spatial orientation and distribution of fibres were shown to be controlled by leucine-rich repeat and IgG domain containing protein 1 (Lingo1) and Nogo receptor 1, which directed the newly formed axons to cortical areas that were otherwise not targeted.72”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
In the rat somatosensory whisker barrel field, ATRX protein contributes to formation of axonal growth cones, which are stabilised by IGF1.
“In the rat somatosensory whisker barrel field, the ATP-dependent DNA-modifying enzyme α-thalassaemia/mental retardation syndrome X-linked (ATRX) protein, which controls neuronal survival and migration during brain development, contributes to the formation of axonal growth cones, which are stabilised by insulin-like growth factor 1.72”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
Expression of plasticity-related proteins in neurons differs between young and old animals.
“Indeed, the expression of plasticity-related proteins in neurons differs between young and old animals.”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
Lingo1 immunostaining was stronger in neurons of old rats (2 years) than young rats (2 months).
“Lingo1 immuno staining, by contrast, was stronger in neurons of old rats (2 years of age) than in young rats (2 months of age).72”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
In periinfarct cortex, IGF-1 was mainly in astrocytes of 2-month-old rats but predominantly neuronal in 2-year-old rats.
“Thus, insulin-like growth factor 1 was localised mainly to astrocytes in the periinfarct cortex of 2-month-old rats, but exhibited predominantly neuronal labelling in 2-year-old rats.72”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
Although evidence is limited, preserved neurological recovery in old animals argues against specific age limits for neurorestorative treatments.
“Although evidence is limited to a rather small number of studies, the preserved neurological recovery in old animals argues against specific age limits for neurorestorative treatments.”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
Although restorative treatments can promote neurological recovery in old animals, specific findings in ageing animals and in animals with vascular risk factors suggest that efficacy of new therapeutics might be compromised in elderly patients with risk factors.
“Although restorative treat ments can promote neurological recovery in old ani mals,17,26,72,76–79 specific findings in ageing animals72,77–79 and in animals with vascular risk factors80,82,86,87 suggest that the efficacy of new therapeutics might be compromised in elderly patients with risk factors.”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [72]
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- Authors
- Li, S., Overman, J. J., Katsman, D., Kozlov, S. V., Donnelly, C. J., Twiss, J. L., Giger, R. J., Coppola, G., Geschwind, D. H., & Carmichael, S. T.
- Affiliations
- University of California, Los Angeles (US)
- Drexel University (US)
- University of Michigan (US)
- Corresponding author
- Carmichael, S Thomas
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2010-11-07
- Volume
- 13
- Issue
- 12
- Pages
- 1496-1504
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3059556
- OpenAlex
- W1981596049
- Cited by
- 329
- References
- 50
- Citations by year
- 2026: 7 · 2025: 14 · 2024: 15 · 2023: 28 · 2022: 17 · 2021: 20 · 2020: 16 · 2019: 34 · 2018: 21 · 2017: 27 · 2016: 20 · 2015: 18 · 2014: 20 · 2013: 20 · 2012: 27
- FWCI
- 9.17
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS049041, R01NS045729, NS045729, R01NS041596, NS04733, R01NS049041)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- axonal sprouting, stroke, epigenetic regulation, growth factors, cell adhesion, axon guidance, cytoskeletal proteins, Eph receptors, neuronal survival, cortical neurons, functional recovery
- MeSH terms
- Aging, Animals, Axons, Cells, Cultured, Male, Mice, Inbred C57BL, Rats, Inbred F344, Sensory Receptor Cells, Up-Regulation, Recovery of Function, Stroke, Gene Expression Profiling, Mice, Rats
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