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Development and Structural Variety of the Chondroitin Sulfate Proteoglycans-Contained Extracellular Matrix in the Mouse Brain.

Horii-Hayashi N, Sasagawa T, Matsunaga W, Nishi M - Neural Plast. (2015)

Bottom Line: In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala.Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms.The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8521, Japan.

ABSTRACT
Chondroitin sulfate proteoglycans (CSPGs) are major components of the extracellular matrix (ECM) in the brain. In adult mammals, CSPGs form the specialized ECM structure perineuronal nets (PNNs) that surround somata and dendrites of certain types of neurons. PNNs restrict synaptic plasticity and regulate the closure of critical periods. Although previous studies have examined the starting period of PNN formation, focusing on primary sensory cortices, there are no systematic studies at the whole brain level. Here, we examined the starting period of PNN formation in male mice ranging in age from postnatal day 3 to week 11, mainly focusing on several cortical areas, limbic structures, hypothalamus, and brain stem, using lectin histochemistry with Wisteria floribunda agglutinin (WFA). Results showed that early PNN formation was observed in several reticular formations of the brain stem related to the cranial nerves and primary somatosensory cortices. In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala. Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms. The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

No MeSH data available.


WFA-stained ECM in the developing hypothalamus. (a–i) WFA-labeled images in the PVN (a–c), LH (d–f), and VMH/Arc (g–i) at P21 (a, d, g), 5 w (b, e, h), and 11 w (c, f, i). Ambiguous PNN-like staining (arrows) was observed in the PVN at P21, which became gradually clear over 5 w to 11 w. PNN-like staining was observed at P21 in the LH, which became clearer at 5 w and 11 w. In all stages shown, WFA reactivity in the VMH was diffuse, while that of the Arc was dense, particularly in its ventral portion neighboring the ME. (j–n) Higher magnification images of WFA labeling at 11 w in the PVN (j), VMH (k), Arc (l), LH (M), and LPO (n). PNN structures in the PVN showed a diffuse manner, while those of the LH and LPO clearly surrounded cell bodies and dendrites. In the VMH and Arc, WFA reactivity did not surround dendrites. Arc: arcuate nucleus; LH: lateral hypothalamus; LPO: lateral preoptic area; ME: median eminence; PVN: paraventricular nucleus; VMH: ventromedial hypothalamic nucleus. Scale bars = 100 (a–f), 400 (g–i), and 40 (j–n) μm.
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fig4: WFA-stained ECM in the developing hypothalamus. (a–i) WFA-labeled images in the PVN (a–c), LH (d–f), and VMH/Arc (g–i) at P21 (a, d, g), 5 w (b, e, h), and 11 w (c, f, i). Ambiguous PNN-like staining (arrows) was observed in the PVN at P21, which became gradually clear over 5 w to 11 w. PNN-like staining was observed at P21 in the LH, which became clearer at 5 w and 11 w. In all stages shown, WFA reactivity in the VMH was diffuse, while that of the Arc was dense, particularly in its ventral portion neighboring the ME. (j–n) Higher magnification images of WFA labeling at 11 w in the PVN (j), VMH (k), Arc (l), LH (M), and LPO (n). PNN structures in the PVN showed a diffuse manner, while those of the LH and LPO clearly surrounded cell bodies and dendrites. In the VMH and Arc, WFA reactivity did not surround dendrites. Arc: arcuate nucleus; LH: lateral hypothalamus; LPO: lateral preoptic area; ME: median eminence; PVN: paraventricular nucleus; VMH: ventromedial hypothalamic nucleus. Scale bars = 100 (a–f), 400 (g–i), and 40 (j–n) μm.

Mentions: In the hypothalamus, WFA labeling patterns and their developmental changes were different within each nucleus or area. In the paraventricular nucleus (PVN), especially in its anterior division, faint PNN-like labeling was observed at P21 (Figure 4(a)), which gradually became clear from 5 w (Figure 4(b)) to 11 w (Figure 4(c)). In the lateral hypothalamus (LH), a comparatively clear PNN-like form was observed at P21 (Figure 4(d)), which became clearer at 5 w (Figure 4(e)) and 11 w (Figure 4(f)). In the ventromedial hypothalamic nucleus (VMH), WFA reactivity was diffusely observed throughout the region at P21 (Figure 4(g)), which became stronger but remained diffuse at 5 w (Figure 4(h)) and 11 w (Figure 4(i)). Contrary to the VMH findings, strong WFA reactivity was observed in the ventral portion of the arcuate nucleus (Arc) neighboring the median eminence (ME) (Figures 4(g)–4(i)). High-power images at 11 w are represented in Figures 4(j)–4(n): PNNs in the PVN surrounded both cell bodies and dendrite-like processes, but they were somewhat diffuse compared with those of the LH (Figure 4(m)) and lateral preoptic area (LPO) (Figure 4(n)). WFA reactivity in the VMH was diffuse and weakly accumulated around particular cell bodies (Figure 4(k)). In the Arc, WFA reactivity densely surrounded cell bodies (Figure 4(l)).


Development and Structural Variety of the Chondroitin Sulfate Proteoglycans-Contained Extracellular Matrix in the Mouse Brain.

Horii-Hayashi N, Sasagawa T, Matsunaga W, Nishi M - Neural Plast. (2015)

WFA-stained ECM in the developing hypothalamus. (a–i) WFA-labeled images in the PVN (a–c), LH (d–f), and VMH/Arc (g–i) at P21 (a, d, g), 5 w (b, e, h), and 11 w (c, f, i). Ambiguous PNN-like staining (arrows) was observed in the PVN at P21, which became gradually clear over 5 w to 11 w. PNN-like staining was observed at P21 in the LH, which became clearer at 5 w and 11 w. In all stages shown, WFA reactivity in the VMH was diffuse, while that of the Arc was dense, particularly in its ventral portion neighboring the ME. (j–n) Higher magnification images of WFA labeling at 11 w in the PVN (j), VMH (k), Arc (l), LH (M), and LPO (n). PNN structures in the PVN showed a diffuse manner, while those of the LH and LPO clearly surrounded cell bodies and dendrites. In the VMH and Arc, WFA reactivity did not surround dendrites. Arc: arcuate nucleus; LH: lateral hypothalamus; LPO: lateral preoptic area; ME: median eminence; PVN: paraventricular nucleus; VMH: ventromedial hypothalamic nucleus. Scale bars = 100 (a–f), 400 (g–i), and 40 (j–n) μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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fig4: WFA-stained ECM in the developing hypothalamus. (a–i) WFA-labeled images in the PVN (a–c), LH (d–f), and VMH/Arc (g–i) at P21 (a, d, g), 5 w (b, e, h), and 11 w (c, f, i). Ambiguous PNN-like staining (arrows) was observed in the PVN at P21, which became gradually clear over 5 w to 11 w. PNN-like staining was observed at P21 in the LH, which became clearer at 5 w and 11 w. In all stages shown, WFA reactivity in the VMH was diffuse, while that of the Arc was dense, particularly in its ventral portion neighboring the ME. (j–n) Higher magnification images of WFA labeling at 11 w in the PVN (j), VMH (k), Arc (l), LH (M), and LPO (n). PNN structures in the PVN showed a diffuse manner, while those of the LH and LPO clearly surrounded cell bodies and dendrites. In the VMH and Arc, WFA reactivity did not surround dendrites. Arc: arcuate nucleus; LH: lateral hypothalamus; LPO: lateral preoptic area; ME: median eminence; PVN: paraventricular nucleus; VMH: ventromedial hypothalamic nucleus. Scale bars = 100 (a–f), 400 (g–i), and 40 (j–n) μm.
Mentions: In the hypothalamus, WFA labeling patterns and their developmental changes were different within each nucleus or area. In the paraventricular nucleus (PVN), especially in its anterior division, faint PNN-like labeling was observed at P21 (Figure 4(a)), which gradually became clear from 5 w (Figure 4(b)) to 11 w (Figure 4(c)). In the lateral hypothalamus (LH), a comparatively clear PNN-like form was observed at P21 (Figure 4(d)), which became clearer at 5 w (Figure 4(e)) and 11 w (Figure 4(f)). In the ventromedial hypothalamic nucleus (VMH), WFA reactivity was diffusely observed throughout the region at P21 (Figure 4(g)), which became stronger but remained diffuse at 5 w (Figure 4(h)) and 11 w (Figure 4(i)). Contrary to the VMH findings, strong WFA reactivity was observed in the ventral portion of the arcuate nucleus (Arc) neighboring the median eminence (ME) (Figures 4(g)–4(i)). High-power images at 11 w are represented in Figures 4(j)–4(n): PNNs in the PVN surrounded both cell bodies and dendrite-like processes, but they were somewhat diffuse compared with those of the LH (Figure 4(m)) and lateral preoptic area (LPO) (Figure 4(n)). WFA reactivity in the VMH was diffuse and weakly accumulated around particular cell bodies (Figure 4(k)). In the Arc, WFA reactivity densely surrounded cell bodies (Figure 4(l)).

Bottom Line: In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala.Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms.The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8521, Japan.

ABSTRACT
Chondroitin sulfate proteoglycans (CSPGs) are major components of the extracellular matrix (ECM) in the brain. In adult mammals, CSPGs form the specialized ECM structure perineuronal nets (PNNs) that surround somata and dendrites of certain types of neurons. PNNs restrict synaptic plasticity and regulate the closure of critical periods. Although previous studies have examined the starting period of PNN formation, focusing on primary sensory cortices, there are no systematic studies at the whole brain level. Here, we examined the starting period of PNN formation in male mice ranging in age from postnatal day 3 to week 11, mainly focusing on several cortical areas, limbic structures, hypothalamus, and brain stem, using lectin histochemistry with Wisteria floribunda agglutinin (WFA). Results showed that early PNN formation was observed in several reticular formations of the brain stem related to the cranial nerves and primary somatosensory cortices. In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala. Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms. The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

No MeSH data available.