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Differential expression of hyperpolarization-activated cyclic nucleotide-gated channel subunits during hippocampal development in the mouse.

Seo H, Seol MJ, Lee K - Mol Brain (2015)

Bottom Line: Each HCN channel isoform showed subfield-specific expression within the hippocampus from postnatal day 7, and only HCN4 was found in glial cells in the stratum lacunosum moleculare at this developmental stage.Furthermore, the immunolabeling for all these isoforms was colocalized with parvalbumin immunolabeling in interneurons of the CA field and in the dentate gyrus.Our mapping data showing the temporal and spatial changes in the expression of HCN channels suggest that HCN1, HCN2, and HCN4 subunits may have distinct physiological roles in the developing hippocampus.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, Brain Science & Engineering Institute, Kyungpook National University Graduate School of Medicine, 2-101, Dongin-dong, Jung-gu, Daegu, 700-842, South Korea. hseo@knu.ac.kr.

ABSTRACT

Background: Hyperpolarization-activated cyclic nucleotide-gated (HCN) channels help control the rhythmic activation of pacemaker neurons during brain development. However, little is known about the timing and cell type specificity of the expression of HCN isoforms during development of the hippocampus.

Results: Here we examined the developmental expression of the brain-enriched HCN1, HCN2, and HCN4 isoforms of HCN channels in mouse hippocampus from embryonic to postnatal stages. All these isoforms were expressed abundantly in the hippocampus at embryonic day 14.5 and postnatal day 0. Each HCN channel isoform showed subfield-specific expression within the hippocampus from postnatal day 7, and only HCN4 was found in glial cells in the stratum lacunosum moleculare at this developmental stage. At postnatal days 21 and 56, all HCN isoforms were strongly expressed in the stratum lacunosum moleculare and the stratum pyramidale of the Cornu Ammonis (CA), as well as in the hilus of the dentate gyrus, but not in the subgranular zone. Furthermore, the immunolabeling for all these isoforms was colocalized with parvalbumin immunolabeling in interneurons of the CA field and in the dentate gyrus.

Conclusions: Our mapping data showing the temporal and spatial changes in the expression of HCN channels suggest that HCN1, HCN2, and HCN4 subunits may have distinct physiological roles in the developing hippocampus.

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Expression of HCN2 in PV-positive cells of the hippocampus at P56. (A-B, D, E-F, H-J, L-N, P): Most PV-immunopositive cells located in the CA1 (A-B, D), CA2 (E, F, H), CA3 (I, J, L), and DG (M, N, P) were labeled with HCN2. (A, E, I): HCN2 expression was most prominent in the sl-m of the CA1 (A), as well as in the sp of the CA2 (E) and CA3 (I). Interestingly, at this stage the alveus showed HCN2 labeling, contrasting with its expression pattern at P21. A-B, D, E-F, H-J, L-N, P: white arrows indicate PV-positive/HCN2-positive cells. C, G, K, O: DAPI staining. Scale bars = 20 μm.
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Fig8: Expression of HCN2 in PV-positive cells of the hippocampus at P56. (A-B, D, E-F, H-J, L-N, P): Most PV-immunopositive cells located in the CA1 (A-B, D), CA2 (E, F, H), CA3 (I, J, L), and DG (M, N, P) were labeled with HCN2. (A, E, I): HCN2 expression was most prominent in the sl-m of the CA1 (A), as well as in the sp of the CA2 (E) and CA3 (I). Interestingly, at this stage the alveus showed HCN2 labeling, contrasting with its expression pattern at P21. A-B, D, E-F, H-J, L-N, P: white arrows indicate PV-positive/HCN2-positive cells. C, G, K, O: DAPI staining. Scale bars = 20 μm.

Mentions: In the CA field of the adult hippocampus, immunolabeled cells for HCN1, HCN2, and HCN4 subunits were found primarily in the SP, and in the SL-M layer (Figures 7, 8 and 9). Comparing the expression of these subunits, the immunolabeling for HCN4 was relatively lower than for HCN1 or HCN2. In the CA1 and CA2, immunoreactivity for HCN1 and HCN2 subunits was more prominent than for HCN4 in the SL-M; while in the SP the expression of HCN1 was relatively higher than that of HCN2 or HCN4 (Figures 7A, E, 8A, E and 9A, E). In the CA3, with the exception of the SL-M, the expression of all HCN subunits was more intense than in the CA1 or CA2 (Figures 7I-J, 8I and 9I). Interestingly, in the alveus, immunolabeling for HCN2 and HCN4 was relatively lower than for HCN1, whereas in earlier stages (i.e., P21) only HCN1 was observed in the alveus (Figures 7, 8, and 9).Figure 7


Differential expression of hyperpolarization-activated cyclic nucleotide-gated channel subunits during hippocampal development in the mouse.

Seo H, Seol MJ, Lee K - Mol Brain (2015)

Expression of HCN2 in PV-positive cells of the hippocampus at P56. (A-B, D, E-F, H-J, L-N, P): Most PV-immunopositive cells located in the CA1 (A-B, D), CA2 (E, F, H), CA3 (I, J, L), and DG (M, N, P) were labeled with HCN2. (A, E, I): HCN2 expression was most prominent in the sl-m of the CA1 (A), as well as in the sp of the CA2 (E) and CA3 (I). Interestingly, at this stage the alveus showed HCN2 labeling, contrasting with its expression pattern at P21. A-B, D, E-F, H-J, L-N, P: white arrows indicate PV-positive/HCN2-positive cells. C, G, K, O: DAPI staining. Scale bars = 20 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4352274&req=5

Fig8: Expression of HCN2 in PV-positive cells of the hippocampus at P56. (A-B, D, E-F, H-J, L-N, P): Most PV-immunopositive cells located in the CA1 (A-B, D), CA2 (E, F, H), CA3 (I, J, L), and DG (M, N, P) were labeled with HCN2. (A, E, I): HCN2 expression was most prominent in the sl-m of the CA1 (A), as well as in the sp of the CA2 (E) and CA3 (I). Interestingly, at this stage the alveus showed HCN2 labeling, contrasting with its expression pattern at P21. A-B, D, E-F, H-J, L-N, P: white arrows indicate PV-positive/HCN2-positive cells. C, G, K, O: DAPI staining. Scale bars = 20 μm.
Mentions: In the CA field of the adult hippocampus, immunolabeled cells for HCN1, HCN2, and HCN4 subunits were found primarily in the SP, and in the SL-M layer (Figures 7, 8 and 9). Comparing the expression of these subunits, the immunolabeling for HCN4 was relatively lower than for HCN1 or HCN2. In the CA1 and CA2, immunoreactivity for HCN1 and HCN2 subunits was more prominent than for HCN4 in the SL-M; while in the SP the expression of HCN1 was relatively higher than that of HCN2 or HCN4 (Figures 7A, E, 8A, E and 9A, E). In the CA3, with the exception of the SL-M, the expression of all HCN subunits was more intense than in the CA1 or CA2 (Figures 7I-J, 8I and 9I). Interestingly, in the alveus, immunolabeling for HCN2 and HCN4 was relatively lower than for HCN1, whereas in earlier stages (i.e., P21) only HCN1 was observed in the alveus (Figures 7, 8, and 9).Figure 7

Bottom Line: Each HCN channel isoform showed subfield-specific expression within the hippocampus from postnatal day 7, and only HCN4 was found in glial cells in the stratum lacunosum moleculare at this developmental stage.Furthermore, the immunolabeling for all these isoforms was colocalized with parvalbumin immunolabeling in interneurons of the CA field and in the dentate gyrus.Our mapping data showing the temporal and spatial changes in the expression of HCN channels suggest that HCN1, HCN2, and HCN4 subunits may have distinct physiological roles in the developing hippocampus.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy, Brain Science & Engineering Institute, Kyungpook National University Graduate School of Medicine, 2-101, Dongin-dong, Jung-gu, Daegu, 700-842, South Korea. hseo@knu.ac.kr.

ABSTRACT

Background: Hyperpolarization-activated cyclic nucleotide-gated (HCN) channels help control the rhythmic activation of pacemaker neurons during brain development. However, little is known about the timing and cell type specificity of the expression of HCN isoforms during development of the hippocampus.

Results: Here we examined the developmental expression of the brain-enriched HCN1, HCN2, and HCN4 isoforms of HCN channels in mouse hippocampus from embryonic to postnatal stages. All these isoforms were expressed abundantly in the hippocampus at embryonic day 14.5 and postnatal day 0. Each HCN channel isoform showed subfield-specific expression within the hippocampus from postnatal day 7, and only HCN4 was found in glial cells in the stratum lacunosum moleculare at this developmental stage. At postnatal days 21 and 56, all HCN isoforms were strongly expressed in the stratum lacunosum moleculare and the stratum pyramidale of the Cornu Ammonis (CA), as well as in the hilus of the dentate gyrus, but not in the subgranular zone. Furthermore, the immunolabeling for all these isoforms was colocalized with parvalbumin immunolabeling in interneurons of the CA field and in the dentate gyrus.

Conclusions: Our mapping data showing the temporal and spatial changes in the expression of HCN channels suggest that HCN1, HCN2, and HCN4 subunits may have distinct physiological roles in the developing hippocampus.

Show MeSH