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Astrocytic Ca2+ signals are required for the functional integrity of tripartite synapses

Tanaka, Mika, Shih, Pei-Yu, Gomi, Hiroshi, Yoshida, Takamasa, Nakai, Junichi, Ando, Reiko, Furuichi, Teiichi, Mikoshiba, Katsuhiko, Semyanov, Alexey, Itohara, Shigeyoshi·2013·Molecular Brain
DOI 10.1186/1756-6606-6-6PMC PMC3563617
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Abstract

Background: Neuronal activity alters calcium ion (Ca 2+) dynamics in astrocytes, but the physiologic relevance of these changes is controversial. To examine this issue further, we generated an inducible transgenic mouse model in which the expression of an inositol 1,4,5-trisphosphate absorbent, “IP 3 sponge”, attenuates astrocytic Ca 2+signaling. Results: Attenuated Ca 2+activity correlated with reduced astrocytic coverage of asymmetric synapses in the hippocampal CA1 region in these animals. The decreased astrocytic ‘protection’ of the synapses facilitated glutamate ‘spillover’, which was reflected by prolonged glutamate transporter currents in stratum radiatum astrocytes and enhanced N-methyl-D-aspartate receptor currents in CA1 pyramidal neurons in response to burst stimulation. These mice also exhibited behavioral impairments in spatial reference memory and remote contextual fear memory, in which hippocampal circuits are involved. Conclusions: Our findings suggest that IP 3-mediated astrocytic Ca 2+signaling correlates with the formation of functional tripartite synapses in the hippocampus.

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Figures

Figure 1 Astrocyte-specific expression of the GST-IP3sponge. (A) Tg1, Tg2 mouse lines were generated. In the DTg mice, expression of the GST-IP3sponge and nls-lacZ is induced under the control of TetO, but can be suppressed by Dox. (B, C) Whole mount lacZ staining of sagittal brains of Tg1 (B) and DTg (C) mice. (D, E) LacZ staining of coronal hippocampal slices of Tg1 (D) and DTg (E) mice. The lacZ expression level in Tg1 was very low (B), but hippocampal dentate gyrus cells showed some leakage (D). Scale bar, 0.5 mm. (F, G) Double immunofluorescence analysis of hippocampal CA1 of DTg mice using antibodies to lacZ, S100B, and NeuN. Insets are magnified images. Scale bar, 100 μm. (H – J) Double immunofluorescence analysis using antibodies to lacZ and GST. Scale bar, 25 μm.
Figure 1 Astrocyte-specific expression of the GST-IP3sponge. (A) Tg1, Tg2 mouse lines were generated. In the DTg mice, expression of the GST-IP3sponge and nls-lacZ is induced under the control of TetO, but can be suppressed by Dox. (B, C) Whole mount lacZ staining of sagittal brains of Tg1 (B) and DTg (C) mice. (D, E) LacZ staining of coronal hippocampal slices of Tg1 (D) and DTg (E) mice. The lacZ expression level in Tg1 was very low (B), but hippocampal dentate gyrus cells showed some leakage (D). Scale bar, 0.5 mm. (F, G) Double immunofluorescence analysis of hippocampal CA1 of DTg mice using antibodies to lacZ, S100B, and NeuN. Insets are magnified images. Scale bar, 100 μm. (H – J) Double immunofluorescence analysis using antibodies to lacZ and GST. Scale bar, 25 μm.CC BY · PubMed Central
Figure 2 Ca2+imaging with G-CaMP2. (A – C) Double immunofluorescence analysis of hippocampal CA1 region from tetO-G-CaMP2:Tg2 (Ctrl) mice using antibodies to G-CaMP2 and S100B. Scale bar, 50 μm. (D – F) Confocal images of double immunofluorescence analysis of hippocampal CA1 of Tg1:tetO-G-CaMP2:Tg2 (TTg) mice using antibodies to G-CaMP2 and lacZ. Scale bar, 100 μm. (G – J) Two-photon images of control (Ctrl) and TTg astrocytes with G-CaMP2 fluorescence. Magenta areas are regions of interest (ROIs) in processes that showed changes in fluorescence over time. Green areas indicate soma. (G) and (H) are the same Ctrl astrocyte and (I) and (J) are the same TTg astrocyte, but under no-puff (G) and (I) and 500-ms puff (H) and (J) conditions. Scale bar, 10 μm. (K – N) Ca2+ traces in the ROIs indicated by arrows and the numbers in (G – J). Red traces in (L) and (N) show changes in the fluorescence induced by 500-ms puff application of Alexa594 with DHPG. Vertical dotted lines in red indicate the onset of puff stimulation. Red asterisks indicate peaks of each Ca2+ event. Vertical and horizontal ranges of gray bands below the asterisks represent the range from the baseline + 1SD to + 2SD and the event duration, respectively. Peaks whose duration could not be identified were excluded from the events. Vertical and horizontal scale bars, respectively, indicate 20% (ΔF/F0) and 20 s. (O, P) Mean (±SEM) duration and mean areas under the curve, respectively, of individual events under no puff, 100-ms puff, and 500-ms puff conditions in Ctrl and TTg groups. A significant increase upon stimulation was observed only in the Ctrl group. *P < 0.05, **P < 0.01, ***P < 0.001, with Bonferroni’s correction for multiple comparisons.
Figure 2 Ca2+imaging with G-CaMP2. (A – C) Double immunofluorescence analysis of hippocampal CA1 region from tetO-G-CaMP2:Tg2 (Ctrl) mice using antibodies to G-CaMP2 and S100B. Scale bar, 50 μm. (D – F) Confocal images of double immunofluorescence analysis of hippocampal CA1 of Tg1:tetO-G-CaMP2:Tg2 (TTg) mice using antibodies to G-CaMP2 and lacZ. Scale bar, 100 μm. (G – J) Two-photon images of control (Ctrl) and TTg astrocytes with G-CaMP2 fluorescence. Magenta areas are regions of interest (ROIs) in processes that showed changes in fluorescence over time. Green areas indicate soma. (G) and (H) are the same Ctrl astrocyte and (I) and (J) are the same TTg astrocyte, but under no-puff (G) and (I) and 500-ms puff (H) and (J) conditions. Scale bar, 10 μm. (K – N) Ca2+ traces in the ROIs indicated by arrows and the numbers in (G – J). Red traces in (L) and (N) show changes in the fluorescence induced by 500-ms puff application of Alexa594 with DHPG. Vertical dotted lines in red indicate the onset of puff stimulation. Red asterisks indicate peaks of each Ca2+ event. Vertical and horizontal ranges of gray bands below the asterisks represent the range from the baseline + 1SD to + 2SD and the event duration, respectively. Peaks whose duration could not be identified were excluded from the events. Vertical and horizontal scale bars, respectively, indicate 20% (ΔF/F0) and 20 s. (O, P) Mean (±SEM) duration and mean areas under the curve, respectively, of individual events under no puff, 100-ms puff, and 500-ms puff conditions in Ctrl and TTg groups. A significant increase upon stimulation was observed only in the Ctrl group. *P < 0.05, **P < 0.01, ***P < 0.001, with Bonferroni’s correction for multiple comparisons.CC BY · PubMed Central
Figure 3 Astrocytic coverage of asymmetric synapses in DTg mice. (A, B) Electron micrographs of the CA1 stratum radiatum of the hippocampus of WT (A) and DTg mice (B). Colors indicate the classification of astrocytic coverage of asymmetric synapses: pink, synapses without astrocytic contact; blue, synapses with astrocytic contact; yellow, astrocytic processes. (C, D) Box-and-whisker plots showing pooled data for percent of synapses without astrocytic contact (each box has lines at the lower quartile, median, and upper quartile values, and whiskers indicating the range). Percent of synapses without astrocytic contact was significantly increased in DTg mice [P = 0.001, Kruskal Wallis test for 3 groups] (C), but was comparable to WT after Dox treatment starting at 1 mo of age (Dox*) [P = 0.012, Kruskal Wallis test for 3 groups] (D). *P < 0.05, **P < 0.01, ***P < 0.001, two-tailed Mann–Whitney U test.
Figure 3 Astrocytic coverage of asymmetric synapses in DTg mice. (A, B) Electron micrographs of the CA1 stratum radiatum of the hippocampus of WT (A) and DTg mice (B). Colors indicate the classification of astrocytic coverage of asymmetric synapses: pink, synapses without astrocytic contact; blue, synapses with astrocytic contact; yellow, astrocytic processes. (C, D) Box-and-whisker plots showing pooled data for percent of synapses without astrocytic contact (each box has lines at the lower quartile, median, and upper quartile values, and whiskers indicating the range). Percent of synapses without astrocytic contact was significantly increased in DTg mice [P = 0.001, Kruskal Wallis test for 3 groups] (C), but was comparable to WT after Dox treatment starting at 1 mo of age (Dox*) [P = 0.012, Kruskal Wallis test for 3 groups] (D). *P < 0.05, **P < 0.01, ***P < 0.001, two-tailed Mann–Whitney U test.CC BY · PubMed Central
Figure 4 Enhanced glutamate spillover in DTg mice. (A) STCs elicited by a single stimulus (black trace) and subtracted traces showing responses to the 5thstimulus (red trace). Insets: STCs are normalized and aligned so that the peaks are superimposed to facilitate comparison of decay. (B) τdecay of STC was not significantly different between WT and DTg mice. n (number of cells) = 16, N (number of animals) = 5 for WT, n = 14, N = 4 for DTg. (C) Frequency dependence of R1/5 decay in WT and DTg mice. n = 5, N = 1 for WT, n = 5, N = 2 for DTg. (D) Representative NMDA currents recorded from CA1 pyramidal neurons in response to a single stimulus (black trace) and trains of stimuli (5 stimuli, 100 Hz, red trace) at +40 mV. Traces induced by 5 stimuli are normalized to the peak amplitude induced by a single stimulus. (E) The ratio of total charge transfer by NMDA receptors (train/single EPSCNMDA area) induced by trains of stimuli to a single stimulus was increased in DTg mice. n = 8, N = 3 for WT, n = 8, N = 4 for DTg. *P < 0.05, unpaired t test. The values on the graphs represent mean ± SEM.
Figure 4 Enhanced glutamate spillover in DTg mice. (A) STCs elicited by a single stimulus (black trace) and subtracted traces showing responses to the 5thstimulus (red trace). Insets: STCs are normalized and aligned so that the peaks are superimposed to facilitate comparison of decay. (B) τdecay of STC was not significantly different between WT and DTg mice. n (number of cells) = 16, N (number of animals) = 5 for WT, n = 14, N = 4 for DTg. (C) Frequency dependence of R1/5 decay in WT and DTg mice. n = 5, N = 1 for WT, n = 5, N = 2 for DTg. (D) Representative NMDA currents recorded from CA1 pyramidal neurons in response to a single stimulus (black trace) and trains of stimuli (5 stimuli, 100 Hz, red trace) at +40 mV. Traces induced by 5 stimuli are normalized to the peak amplitude induced by a single stimulus. (E) The ratio of total charge transfer by NMDA receptors (train/single EPSCNMDA area) induced by trains of stimuli to a single stimulus was increased in DTg mice. n = 8, N = 3 for WT, n = 8, N = 4 for DTg. *P < 0.05, unpaired t test. The values on the graphs represent mean ± SEM.CC BY · PubMed Central
Figure 5 Behavioral impairments in DTg mice. (A – C) Morris water maze test. Acquisition rates in the hidden platform task did not significantly differ between DTg mice and WT mice (A, N = 23 for WT, N = 24 for DTg), but DTg mice spent significantly less time in the target quadrant during the probe test than did WT mice (B). Dashed line indicates chance level. No difference was observed between genotypes in the visible platform task (C). (D, E) DTg mice treated with Dox (DTg Dox) were not impaired in the hidden platform task (D) or probe test (E, N = 24/genotype). (F – H) Fear-conditioning and footshock sensitivity test. (F, G) Each column represents mean percent time freezing during the last 2-min recording period for conditioning, 5-min recording for contextual test, and the last 3-min recording period for cued test. DTg mice showed normal contextual and cued fear memory at 1 d and 2 d after conditioning, respectively (F). In contrast, DTg mice exhibited significantly reduced remote contextual fear memory at 30 d after conditioning (G), whereas they showed normal remote cued fear memory (G) and footshock sensitivity (H, N = 12 for each genotype). (I – K) DTg mice treated with Dox were not impaired in recent (I) or remote (J) fear memory, or footshock sensitivity (K, N = 12 for each genotype). *P < 0.05, **P < 0.01, unpaired t test. Results are provided as mean ± SEM. Flinch, animal flinched; Vocal, animal vocalized; S jump, small jump; B jump, big jump.
Figure 5 Behavioral impairments in DTg mice. (A – C) Morris water maze test. Acquisition rates in the hidden platform task did not significantly differ between DTg mice and WT mice (A, N = 23 for WT, N = 24 for DTg), but DTg mice spent significantly less time in the target quadrant during the probe test than did WT mice (B). Dashed line indicates chance level. No difference was observed between genotypes in the visible platform task (C). (D, E) DTg mice treated with Dox (DTg Dox) were not impaired in the hidden platform task (D) or probe test (E, N = 24/genotype). (F – H) Fear-conditioning and footshock sensitivity test. (F, G) Each column represents mean percent time freezing during the last 2-min recording period for conditioning, 5-min recording for contextual test, and the last 3-min recording period for cued test. DTg mice showed normal contextual and cued fear memory at 1 d and 2 d after conditioning, respectively (F). In contrast, DTg mice exhibited significantly reduced remote contextual fear memory at 30 d after conditioning (G), whereas they showed normal remote cued fear memory (G) and footshock sensitivity (H, N = 12 for each genotype). (I – K) DTg mice treated with Dox were not impaired in recent (I) or remote (J) fear memory, or footshock sensitivity (K, N = 12 for each genotype). *P < 0.05, **P < 0.01, unpaired t test. Results are provided as mean ± SEM. Flinch, animal flinched; Vocal, animal vocalized; S jump, small jump; B jump, big jump.CC BY · PubMed Central
Figure 6 Involvement of astrocytic Ca2+in tripartite synapses. (A) Control astrocytes. (B) IP3 sponge-expressing astrocytes. Suppression of Ca2+ activity in IP3 sponge-expressing astrocytes leads to retraction of astrocytic processes from the synapse, which moves astrocytic glutamate transporters further away and allows for more glutamate spillover.
Figure 6 Involvement of astrocytic Ca2+in tripartite synapses. (A) Control astrocytes. (B) IP3 sponge-expressing astrocytes. Suppression of Ca2+ activity in IP3 sponge-expressing astrocytes leads to retraction of astrocytic processes from the synapse, which moves astrocytic glutamate transporters further away and allows for more glutamate spillover.CC BY · PubMed Central

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Metadata

Authors
Tanaka, M., Shih, P.-Y., Gomi, H., Yoshida, T., Nakai, J., Ando, R., Furuichi, T., Mikoshiba, K., Semyanov, A., & Itohara, S.
Venue
Molecular Brain
Publisher
Springer Science and Business Media LLC
Published
2013-01-28
Volume
6
Issue
1
ISSN
1756-6606
DOI
10.1186/1756-6606-6-6
PMC
PMC3563617
Cited by
127
References
5
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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