Environmental enrichment upregulates striatal synaptic vesicle-associated proteins and improves motor function

Suk Young Song, Minji Chae, Ji Hea Yu, Min Young Lee, Soonil Pyo, Yoon Kyum Shin, Ahreum Baek, Jungwon Park, Eun Sook Park, Ja Young Choi, Sung-Rae Cho

Research output: Contribution to journalArticle

Abstract

Environmental enrichment (EE) is a therapeutic paradigm that consists of complex combinations of physical, cognitive, and social stimuli. The mechanisms underlying EE-mediated synaptic plasticity have yet to be fully elucidated. In this study, we investigated the effects of EE on synaptic vesicle-associated proteins and whether the expression of these proteins is related to behavioral outcomes. A total of 44 CD-1® (ICR) mice aged 6 weeks were randomly assigned to either standard cages or EE (N = 22 each). Rotarod and ladder walking tests were then performed to evaluate motor function. To identify the molecular mechanisms underlying the effects of EE, we assessed differentially expressed proteins (DEPs) in the striatum by proteomic analysis. Quantitative real-time polymerase chain reaction (qRT-PCR), western blot, and immunohistochemistry were conducted to validate the expressions of these proteins. In the behavioral assessment, EE significantly enhanced performance on the rotarod and ladder walking tests. A total of 116 DEPs (54 upregulated and 62 downregulated proteins) were identified in mice exposed to EE. Gene ontology (GO) analysis demonstrated that the upregulated proteins in EE mice were primarily related to biological processes of synaptic vesicle transport and exocytosis. The GO terms for these biological processes commonly included Synaptic vesicle glycoprotein 2B (SV2B), Rabphilin-3A, and Piccolo. The qRT-PCR and western blot analyses revealed that EE increased the expression of SV2B, Rabphilin-3A and Piccolo in the striatum compared to the control group. Immunohistochemistry showed that the density of Piccolo in the vicinity of the subventricular zone was significantly increased in the EE mice compared with control mice. In conclusion, EE upregulates proteins associated with synaptic vesicle transport and exocytosis such as SV2B, Rabphilin-3A and Piccolo in the striatum. These upregulated proteins may be responsible for locomotor performance improvement, as shown in rotarod and ladder walking tests. Elucidation of these changes in synaptic protein expression provides new insights into the mechanism and potential role of EE.

Original languageEnglish
Article number465
JournalFrontiers in Neurology
Volume9
Issue numberJUL
DOIs
Publication statusPublished - 2018 Jul 16

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Corpus Striatum
Synaptic Vesicles
Up-Regulation
Proteins
Walking
Biological Phenomena
Glycoproteins
Gene Ontology
Exocytosis
Real-Time Polymerase Chain Reaction
Western Blotting
Immunohistochemistry
Inbred ICR Mouse
Neuronal Plasticity
Lateral Ventricles
Proteomics
Down-Regulation
Control Groups

All Science Journal Classification (ASJC) codes

  • Neurology
  • Clinical Neurology

Cite this

Song, Suk Young ; Chae, Minji ; Yu, Ji Hea ; Lee, Min Young ; Pyo, Soonil ; Shin, Yoon Kyum ; Baek, Ahreum ; Park, Jungwon ; Park, Eun Sook ; Choi, Ja Young ; Cho, Sung-Rae. / Environmental enrichment upregulates striatal synaptic vesicle-associated proteins and improves motor function. In: Frontiers in Neurology. 2018 ; Vol. 9, No. JUL.
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abstract = "Environmental enrichment (EE) is a therapeutic paradigm that consists of complex combinations of physical, cognitive, and social stimuli. The mechanisms underlying EE-mediated synaptic plasticity have yet to be fully elucidated. In this study, we investigated the effects of EE on synaptic vesicle-associated proteins and whether the expression of these proteins is related to behavioral outcomes. A total of 44 CD-1{\circledR} (ICR) mice aged 6 weeks were randomly assigned to either standard cages or EE (N = 22 each). Rotarod and ladder walking tests were then performed to evaluate motor function. To identify the molecular mechanisms underlying the effects of EE, we assessed differentially expressed proteins (DEPs) in the striatum by proteomic analysis. Quantitative real-time polymerase chain reaction (qRT-PCR), western blot, and immunohistochemistry were conducted to validate the expressions of these proteins. In the behavioral assessment, EE significantly enhanced performance on the rotarod and ladder walking tests. A total of 116 DEPs (54 upregulated and 62 downregulated proteins) were identified in mice exposed to EE. Gene ontology (GO) analysis demonstrated that the upregulated proteins in EE mice were primarily related to biological processes of synaptic vesicle transport and exocytosis. The GO terms for these biological processes commonly included Synaptic vesicle glycoprotein 2B (SV2B), Rabphilin-3A, and Piccolo. The qRT-PCR and western blot analyses revealed that EE increased the expression of SV2B, Rabphilin-3A and Piccolo in the striatum compared to the control group. Immunohistochemistry showed that the density of Piccolo in the vicinity of the subventricular zone was significantly increased in the EE mice compared with control mice. In conclusion, EE upregulates proteins associated with synaptic vesicle transport and exocytosis such as SV2B, Rabphilin-3A and Piccolo in the striatum. These upregulated proteins may be responsible for locomotor performance improvement, as shown in rotarod and ladder walking tests. Elucidation of these changes in synaptic protein expression provides new insights into the mechanism and potential role of EE.",
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Environmental enrichment upregulates striatal synaptic vesicle-associated proteins and improves motor function. / Song, Suk Young; Chae, Minji; Yu, Ji Hea; Lee, Min Young; Pyo, Soonil; Shin, Yoon Kyum; Baek, Ahreum; Park, Jungwon; Park, Eun Sook; Choi, Ja Young; Cho, Sung-Rae.

In: Frontiers in Neurology, Vol. 9, No. JUL, 465, 16.07.2018.

Research output: Contribution to journalArticle

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T1 - Environmental enrichment upregulates striatal synaptic vesicle-associated proteins and improves motor function

AU - Song, Suk Young

AU - Chae, Minji

AU - Yu, Ji Hea

AU - Lee, Min Young

AU - Pyo, Soonil

AU - Shin, Yoon Kyum

AU - Baek, Ahreum

AU - Park, Jungwon

AU - Park, Eun Sook

AU - Choi, Ja Young

AU - Cho, Sung-Rae

PY - 2018/7/16

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N2 - Environmental enrichment (EE) is a therapeutic paradigm that consists of complex combinations of physical, cognitive, and social stimuli. The mechanisms underlying EE-mediated synaptic plasticity have yet to be fully elucidated. In this study, we investigated the effects of EE on synaptic vesicle-associated proteins and whether the expression of these proteins is related to behavioral outcomes. A total of 44 CD-1® (ICR) mice aged 6 weeks were randomly assigned to either standard cages or EE (N = 22 each). Rotarod and ladder walking tests were then performed to evaluate motor function. To identify the molecular mechanisms underlying the effects of EE, we assessed differentially expressed proteins (DEPs) in the striatum by proteomic analysis. Quantitative real-time polymerase chain reaction (qRT-PCR), western blot, and immunohistochemistry were conducted to validate the expressions of these proteins. In the behavioral assessment, EE significantly enhanced performance on the rotarod and ladder walking tests. A total of 116 DEPs (54 upregulated and 62 downregulated proteins) were identified in mice exposed to EE. Gene ontology (GO) analysis demonstrated that the upregulated proteins in EE mice were primarily related to biological processes of synaptic vesicle transport and exocytosis. The GO terms for these biological processes commonly included Synaptic vesicle glycoprotein 2B (SV2B), Rabphilin-3A, and Piccolo. The qRT-PCR and western blot analyses revealed that EE increased the expression of SV2B, Rabphilin-3A and Piccolo in the striatum compared to the control group. Immunohistochemistry showed that the density of Piccolo in the vicinity of the subventricular zone was significantly increased in the EE mice compared with control mice. In conclusion, EE upregulates proteins associated with synaptic vesicle transport and exocytosis such as SV2B, Rabphilin-3A and Piccolo in the striatum. These upregulated proteins may be responsible for locomotor performance improvement, as shown in rotarod and ladder walking tests. Elucidation of these changes in synaptic protein expression provides new insights into the mechanism and potential role of EE.

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