Increased synthesis of chondroitin sulfate proteoglycan promotes adult hippocampal neurogenesis in response to enriched environment
Open accessAbstract
Chondroitin sulfate proteoglycan (CSPG) is a candidate regulator of embryonic neurogenesis. The aim of this study was to specify the functional significance of CSPG in adult hippocampal neurogenesis using male mice. Here, we showed that neural stem cells and neuronal progenitors in the dentate gyrus were covered in part by CSPG. Pharmacological depletion of CSPG in the dentate gyrus reduced the densities of neuronal progenitors and newborn granule cells. 3D reconstruction of newborn granule cells showed that their maturation was inhibited by CSPG digestion. The novel object recognition test revealed that CSPG digestion caused cognitive memory impairment. Western blot analysis showed that expression of β-catenin in the dentate gyrus was decreased by CSPG digestion. The amount of CSPG in the dentate gyrus was increased by enriched environment (EE) and was decreased by forced swim stress. In addition, EE accelerated the recovery of CSPG expression in the dentate gyrus from the pharmacological depletion and promoted the restoration of granule cell production. Conversely, the densities of newborn granule cells were also decreased in mice that lacked chondroitin sulfateN-acetylgalactosaminyltransferase 1 (CSGalNAcT1), a key enzyme for CSPG synthesis (T1KO mice). The capacity of EE to promote granule cell production and improve cognitive memory was impaired in T1KO mice. These findings indicate that CSPG is involved in the regulation of adult hippocampal neurogenesis and suggest that increased synthesis of CSPG by CSGalNacT1 may mediate promotion of granule cell production and improvement of cognitive memory in response to EE. SIGNIFICANCE STATEMENTChondroitin sulfate proteoglycan (CSPG) is a candidate regulator of embryonic neurogenesis. Here, we specified the role of CSPG in adult neurogenesis in the mouse hippocampus. Digestion of CSPG in the dentate gyrus impaired granule cell production and cognitive memory. Enriched environment (EE) promoted the recovery of CSPG expression and granule cell production from the CSPG digestion. Additionally, adult neurogenesis was impaired in mice that lacked a key enzyme for CSPG synthesis (T1KO mice). The capacity of EE to promote granule cell production and cognitive memory was impaired in T1KO mice. Altogether, these findings indicate that CSPG underlies adult hippocampal neurogenesis and suggest that increased synthesis of CSPG may mediate promotion of granule cell production in response to EE.
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Depletion of chondroitin sulfate proteoglycans in the hippocampus decreases new neuron formation and dendritic tree maturation, and produces cognitive impairment.
“Depletion of chondroitin sulfate proteoglycans in the hippocampus decreases new neuron formation and dendritic tree maturation, and produces cognitive impairment (Figure 3A).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Yamada et al., 2018
Chondroitin sulfate proteoglycans surround new neurons in the hippocampus and are important for the production and differentiation of new neurons in adulthood.
“Chondroitin sulfate proteoglycans, structural ECM components, are known to surround new neurons in the hippocampus, and recent work has shown that this molecule is important for the production and differentiation of new neurons in adulthood (Yamada et al., 2018).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Yamada et al., 2018
Environmental enrichment-induced increases in adult neurogenesis are associated with increased synthesis of chondroitin sulfate proteoglycans, which is prevented by chondroitin sulfate proteoglycan synthesis disruption.
“Environmental enrichment-induced increases in adult neurogenesis are associated with increased synthesis of chondroitin sulfate proteoglycans, which is prevented by chondroitin sulfate proteoglycan synthesis disruption (Yamada et al., 2018).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Yamada et al., 2018
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Matrisome Transcriptome Dynamics during Tissue Aging
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The Neurogenic potential of stem cells is altered in Mucopolysaccharidosis type IIIA
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- Authors
- Yamada, J., Nadanaka, S., Kitagawa, H., Takeuchi, K., & Jinno, S.
- Affiliations
- Kyushu University (JP)
- Kobe Pharmaceutical University (JP)
- Aichi Medical University (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2018-08-20
- Volume
- 38
- Issue
- 39
- Pages
- 8496-8513
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6596167
- OpenAlex
- W2888107430
- Cited by
- 38
- References
- 68
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 4 · 2023: 4 · 2022: 8 · 2021: 4 · 2020: 6 · 2019: 6
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (16H05088, 15H04267, 17K07353)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- chondroitin sulfate proteoglycans, adult hippocampal neurogenesis, environmental enrichment, dentate gyrus, cognitive memory, β-catenin, forced swim stress, neural stem cells, neuronal precursors
- MeSH terms
- Animals, Cognition, Environment, Hippocampus, Male, Memory, Mice, Inbred C57BL, Neurons, Chondroitin Sulfate Proteoglycans, N-Acetylgalactosaminyltransferases, Mice, Knockout, Recognition, Psychology, Neurogenesis, Neural Stem Cells
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