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Research ArticleResearch Article: New Research, Disorders of the Nervous System

Developmental Changes in Dendritic Spine Morphology in the Striatum and Their Alteration in an A53T α-Synuclein Transgenic Mouse Model of Parkinson’s Disease

Laxmi Kumar Parajuli, Ken Wako, Suiki Maruo, Soichiro Kakuta, Tomoyuki Taguchi, Masashi Ikuno, Hodaka Yamakado, Ryosuke Takahashi and Masato Koike
eNeuro 17 August 2020, 7 (4) ENEURO.0072-20.2020; DOI: https://doi.org/10.1523/ENEURO.0072-20.2020
Laxmi Kumar Parajuli
1Department of Cell Biology and Neuroscience, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan
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Ken Wako
1Department of Cell Biology and Neuroscience, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan
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Suiki Maruo
1Department of Cell Biology and Neuroscience, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan
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Soichiro Kakuta
2Department of Cellular and Molecular Neuropathology, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan
3Laboratory of Morphology and Image Analysis, Research Support Center, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan
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Tomoyuki Taguchi
4Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
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Masashi Ikuno
4Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
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Hodaka Yamakado
4Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
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Ryosuke Takahashi
4Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto 606-8507, Japan
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Masato Koike
1Department of Cell Biology and Neuroscience, Juntendo University Graduate School of Medicine, Tokyo 113-8421, Japan
5Advanced Research Institute for Health Science, Juntendo University, Tokyo 113-8421, Japan
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    Figure 1.

    3D reconstruction of dendrites and spines from WT and A53T-BAC-SNCA mice at different ages. A, Membrane contours of dendrites (d), spines (s), and presynaptic terminals (t) can be clearly observed in the FIB/SEM image from a 1-month-old WT mouse. Mitochondria and other organelles are also clearly visible. Scale bar: 500 nm. B–I, 3D reconstruction of dendrites (orange) and spines (violet) from WT mice at 1 (B), 3 (C), 6 (D), and 22 (E) months of age and from A53T-BAC-SNCA mice at 1 (F), 3 (G), 6 (H), and 22 (I) months of age. Red regions in the spine heads indicate postsynaptic densities. Scale cubes: 0.5 µm on each side.

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    Figure 2.

    Morphologic alterations in spines in WT and A53T-BAC-SNCA mice with age. A, Age-related changes in spine density. The graph shows that spine density decreased with age in both the WT and A53T-BAC-SNCA mice. In WT mice, the spine density at 1 and 3 months was significantly lower compared with that at 6 and 22 months (**p = 0.003 between 1 and 6 months, ***p < 0.001 between 1 and 22 months, *p = 0.03 between 3 and 6 months, **p = 0.001 between 3 and 22 months; one-way ANOVA). In A53T-BAC-SNCA mice, there were fewer spines at 22 months compared with that at 1 and 3 months (*p = 0.01 between 1 and 22 months, *p = 0.01 between 3 and 22 months; Kruskal–Wallis test). B, Age-related changes in spine head volume. The average spine head volume increases with age in the WT (red open circle), but not A53T-BAC-SNCA (black open circle), mice. In WT mice, spine head volume at 1 month was significantly smaller than that at 3, 6, and 22 months (***p < 0.001 between 1 and 3 months, ***p < 0.001 between 1 and 6 months, ***p < 0.001 between 1 and 22 months; Kruskal–Wallis test). Median head volume is shown by the + symbol. C, Age-related changes in spine neck length. The spine neck length did not vary significantly with age in either WT or A53T-BAC-SNCA mice. Different levels of significance are denoted by the number of asterisks (*p <0.05, **p <0.01, ***p <0.001).

  • Figure 3.
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    Figure 3.

    The frequency of large spines increased with age in WT, but not A53T-BAC-SNCA, mice. A, The distribution of large spines in WT mice was significantly different between 6 and 22 months of age (*p = 0.01, Kolmogorov–Smirnov test). B, In contrast, the distribution of large spines was not significantly different between 6 and 22 months of age in A53T-BAC-SNCA mice (p = 0.86, Kolmogorov–Smirnov test).

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    Figure 4.

    Examples of perforated spines in WT mice at 22 months of age. A–D, Serial images of a large spine (s). Arrows in B, C show the discontinuity of the PSD. Scale bars: 500 nm. E–G, Representative images of a 3D reconstruction of spines showing a doughnut-shaped perforated PSD with a hole at the center. Spine heads, spine necks, and PSDs are shown in violet, blue, and red, respectively. Scale cubes: 0.25 µm on each side.

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    Figure 5.

    PSD area was correlated with spine head volume in both WT and A53T-BAC-SNCA mice. A–H, A significant, positive linear correlation exists between PSDs and spine head volumes in both WT (A, C, E, G) and A53T-BAC-SNCA (B, D, F, H) mice at all four examined ages [1 month (A, B); 3 months (C, D); 6 months (E, F); 22 months (G, H)]. The correlation coefficients and the p values for the test of statistical significance of correlation are denoted by r and p, respectively, in the corresponding graphs. Correlation was examined using Spearman’s rank order test.

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    Figure 6.

    Localization of phosphorylated α-synuclein in a subset of presynaptic terminals in A53T-BAC-SNCA mice. A–D, TEM images of pre-embedding immunogold-labeled samples from A53T-BAC-SNCA mice at 1 (A), 3 (B), 6 (C), and 22 (D) months. Note that the immunogold particles, indicating phosphorylated α-synuclein, were predominantly localized to presynaptic terminals. Immunogold particles were often seen in clusters. E, A low-magnification image from an A53T-BAC-SNCA mouse at 3 months of age demonstrates that a subset of large presynaptic terminals was immunopositive for phosphorylated α-synuclein. s: spine; T: presynaptic terminals with immunoreactivity for phosphorylated α-synuclein; t: presynaptic terminals lacking immunoreactivity for phosphorylated α-synuclein. Scale bars: 500 nm.

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Developmental Changes in Dendritic Spine Morphology in the Striatum and Their Alteration in an A53T α-Synuclein Transgenic Mouse Model of Parkinson’s Disease
Laxmi Kumar Parajuli, Ken Wako, Suiki Maruo, Soichiro Kakuta, Tomoyuki Taguchi, Masashi Ikuno, Hodaka Yamakado, Ryosuke Takahashi, Masato Koike
eNeuro 17 August 2020, 7 (4) ENEURO.0072-20.2020; DOI: 10.1523/ENEURO.0072-20.2020

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Developmental Changes in Dendritic Spine Morphology in the Striatum and Their Alteration in an A53T α-Synuclein Transgenic Mouse Model of Parkinson’s Disease
Laxmi Kumar Parajuli, Ken Wako, Suiki Maruo, Soichiro Kakuta, Tomoyuki Taguchi, Masashi Ikuno, Hodaka Yamakado, Ryosuke Takahashi, Masato Koike
eNeuro 17 August 2020, 7 (4) ENEURO.0072-20.2020; DOI: 10.1523/ENEURO.0072-20.2020
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Keywords

  • α-synuclein
  • A53T
  • dendrite
  • dendritic spines
  • FIB/SEM
  • Parkinson’s disease

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