Abolition of aberrant neurogenesis ameliorates cognitive impairment after stroke in mice

Cuartero, María Isabel; de la Parra, Juan; Pérez-Ruiz, Alberto; Bravo-Ferrer, Isabel; Durán-Laforet, Violeta; García-Culebras, Alicia; García-Segura, Juan Manuel; Dhaliwal, Jagroop; Frankland, Paul W.; Lizasoain, Ignacio; Moro, María Ángeles

doi:10.1172/jci120412

Cited by 128Neurogenesis and neuroplasticity mechanismsMemory and Neural MechanismsNeurological Disease Mechanisms and Treatments

Abolition of aberrant neurogenesis ameliorates cognitive impairment after stroke in mice

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Cuartero, María Isabel, de la Parra, Juan, Pérez-Ruiz, Alberto, Bravo-Ferrer, Isabel, Durán-Laforet, Violeta, García-Culebras, Alicia, García-Segura, Juan Manuel, Dhaliwal, Jagroop +3 more·2019·Journal of Clinical Investigation

DOI 10.1172/jci120412PMC PMC6436875

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Abstract

Poststroke cognitive impairment is considered one of the main complications during the chronic phase of ischemic stroke. In the adult brain, the hippocampus regulates both encoding and retrieval of new information through adult neurogenesis. Nevertheless, the lack of predictive models and studies based on the forgetting processes hinders the understanding of memory alterations after stroke. Our aim was to explore whether poststroke neurogenesis participates in the development of long-term memory impairment. Here, we show a hippocampal neurogenesis burst that persisted 1 month after stroke and that correlated with an impaired contextual and spatial memory performance. Furthermore, we demonstrate that the enhancement of hippocampal neurogenesis after stroke by physical activity or memantine treatment weakened existing memories. More importantly, stroke-induced newborn neurons promoted an aberrant hippocampal circuitry remodeling with differential features at ipsi- and contralesional levels. Strikingly, inhibition of stroke-induced hippocampal neurogenesis by temozolomide treatment or using a genetic approach (Nestin-CreERT2/NSE-DTA mice) impeded the forgetting of old memories. These results suggest that hippocampal neurogenesis modulation could be considered as a potential approach for treatment of poststroke cognitive impairment.

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Brain injury models such as stroke, seizure, and blunt trauma all increase the rate of adult neurogenesis, yet each of these conditions is associated with reduced cognitive function.
“Brain injury models, such as stroke, seizure, and blunt trauma, all increase the rate of adult neurogenesis (Table 1), yet each of these conditions is associated with reduced cognitive function (Cuartero et al., 2019; Parent and Lowenstein, 2002; Sun et al., 2015).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Cuartero et al., 2019
Inhibiting adult neurogenesis reduces the frequency of chronic seizures along with seizure-related cognitive decline as well as stroke-induced cognitive decline.
“In fact, inhibiting adult neurogenesis reduces the frequency of chronic seizures along with seizure-related cognitive decline (Cho et al., 2015) as well as stroke-induced cognitive decline (Cuartero et al., 2019).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Cuartero et al., 2019

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Increased serum QUIN/KYNA is a reliable biomarker of post-stroke cognitive decline
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Electroacupuncture Ameliorates Depression-Like Behaviors Comorbid to Chronic Neuropathic Pain via Tet1-Mediated Restoration of Adult Neurogenesis
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Voluntary Exercise Increases Neurogenesis and Mediates Forgetting of Complex Paired Associates Memories
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HDAC6 dysfunction contributes to impaired maturation of adult neurogenesis in vivo: vital role on functional recovery after ischemic stroke
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Endogenous neural precursor cells in health and disease
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Long Non-coding RNA ANRIL Downregulation Alleviates Neuroinflammation in an Ischemia Stroke Model via Modulation of the miR-671-5p/NF-κB Pathway
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Brain-Derived Estrogen Regulates Neurogenesis, Learning and Memory with Aging in Female Rats
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Repeated oxytocin treatment during abstinence inhibited context- or restraint stress-induced reinstatement of methamphetamine-conditioned place preference and promoted adult hippocampal neurogenesis in mice
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Chaperone-mediated autophagy (CMA) alleviates cognitive impairment by reducing neuronal death in sepsis-associated encephalopathy (SAE)
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Growth Hormone Treatment Promotes Remote Hippocampal Plasticity after Experimental Cortical Stroke
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Circadian Control of Neutrophils Drives Collateral Perfusion and Stroke Outcome
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Brain‐associated innate leukocytes display diverse inflammatory states following experimental stroke
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Delayed rFGF21 Administration Improves Cerebrovascular Remodeling and White Matter Repair After Focal Stroke in Diabetic Mice
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Post-Stroke Social Isolation Reduces Cell Proliferation in the Dentate Gyrus and Alters miRNA Profiles in the Aged Female Mice Brain
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Defective hippocampal neurogenesis underlies cognitive impairment by carotid stenosis-induced cerebral hypoperfusion in mice
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CCN1 Is a Therapeutic Target for Reperfused Ischemic Brain Injury
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Induction of mitochondrial biogenesis enhances neurogenesis and cognitive recovery following ischaemic stroke
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Caveolin-1 Derived from Brain Microvascular Endothelial Cells Inhibits Neuronal Differentiation of Neural Stem/Progenitor Cells In Vivo and In Vitro
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Pathological Nuclear Hallmarks in Dentate Granule Cells of Alzheimer’s Patients: A Biphasic Regulation of Neurogenesis
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Phosphofructokinase-1 Inhibition Promotes Neuronal Differentiation of Neural Stem Cells and Functional Recovery After Stroke
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Adult neurogenesis mediates forgetting of multiple types of memory in the ratPreprint
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Sodium oligomannate modulates the gut-brain axis to alleviate post-stroke cognitive impairment by restoring butyrate metabolism
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Neural recovery after cortical injury: Effects of MSC derived extracellular vesicles on motor circuit remodeling in rhesus monkeys
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Neurogenesis-mediated circuit remodeling reduces engram reinstatement and promotes forgettingPreprint
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Blockade of D-serine signaling and adult hippocampal neurogenesis attenuates remote contextual fear memory following multiple memory retrievals in male mice
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Accelerated long-term forgetting across neuropsychiatric disorders: A review of mechanisms and a neurobiological perspective of forgetting
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Decreased hippocampal neurogenesis and post-stroke depression
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The microglia-derived protein Sema4ab attenuates regenerative neurogenesis after spinal cord injury in zebrafish
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Neuroprotective Effects, Mechanisms of Action and Therapeutic Potential of the Kv7/KCNQ Channel Opener QO-83 in Ischemic Stroke
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Running ameliorates methamphetamine-associated cognitive impairment by regulating hippocampal neurogenesis through the GSK3β/β-catenin pathway
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Oxytocin attenuates the retrieval of methamphetamine-associated reward memories by enhancing adult hippocampal neurogenesis in mice
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Inhibiting aberrant seizure-induced neurogenesis by temozolomide improves cognitive impairments associated with long-term amygdala kindling
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Authors: Cuartero, M. I., de la Parra, J., Pérez-Ruiz, A., Bravo-Ferrer, I., Durán-Laforet, V., García-Culebras, A., García-Segura, J. M., Dhaliwal, J., Frankland, P. W., Lizasoain, I., & Moro, M. Á.
Affiliations: Universidad Complutense de Madrid (ES)
Hospital for Sick Children (CA)
ORCID: Cuartero, María Isabel
de la Parra, Juan
García-Segura, Juan Manuel
Frankland, Paul W.
Moro, María Ángeles
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2019-02-25
Volume: 129
Issue: 4
Pages: 1536-1550
ISSN: 0021-9738 (ISSN-L)
1558-8238
DOI: 10.1172/jci120412
PMC: PMC6436875
OpenAlex: W2913288555
Cited by: 128
References: 69
Citations by year: 2026: 15 · 2025: 17 · 2024: 8 · 2023: 23 · 2022: 18 · 2021: 18 · 2020: 18 · 2019: 11
FWCI: 6.12
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Clinical Investigation (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Funders: Ministerio de Economía y Competitividad (SAF2015-68632-R)
Canadian Institutes of Health Research (143227_1)
Instituto de Salud Carlos III (PI17/01601)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Neurology › Neurological Disease Mechanisms and Treatments
Keywords: post-stroke cognitive impairment, ischemic stroke, forgetting, contextual memory, spatial memory, physical activity, memantine, temozolomide, newborn neurons, therapeutic target
MeSH terms: Temozolomide, Animals, Hippocampus, Male, Mice, Transgenic, Stroke, Mice, Neurogenesis, Cognitive Dysfunction, Spatial Memory

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Abolition of aberrant neurogenesis ameliorates cognitive impairment after stroke in mice

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