Laminar distribution of synaptopodin in normal and reeler mouse brain depends on the position of spine‐bearing neurons

Deller, Thomas; Haas, Carola A.; Deissenrieder, Kathrin; Turco, Domenico Del; Coulin, Carola; Gebhardt, Carl; Drakew, Alexander; Schwarz, Karin; Mündel, Peter; Frotscher, Michael

doi:10.1002/cne.10362

Cited by 14 publications

(27 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…SP has been associated with the spine apparatus, a membranous extension of the dendritic smooth endoplasmic reticulum. This neuronal organelle is found in a subpopulation of spines of telencephalic neurons (Spacek, 1985;Spacek and Harris, 1997) and, interestingly, its regional distribution pattern mirrors the expression pattern of SP (Mundel et al, 1997;Deller et al, 2000Deller et al, , 2002. Using immunogold-EM analysis, SP-immunoreactivity was found in close association with the spine apparatus (Deller et al, 2000(Deller et al, , 2003.…”

Section: Discussionmentioning

confidence: 98%

Synaptopodin Regulates Plasticity of Dendritic Spines in Hippocampal Neurons

Vlachos

Korkotian²,

Schonfeld³

et al. 2009

J. Neurosci.

171

217

View full text Add to dashboard Cite

The spine apparatus is an essential component of dendritic spines of cortical and hippocampal neurons, yet its functions are still enigmatic. Synaptopodin (SP), an actin-binding protein, is tightly associated with the spine apparatus and it may play a role in synaptic plasticity, but it has not yet been linked mechanistically to synaptic functions. We studied endogenous and transfected SP in dendritic spines of cultured hippocampal neurons and found that spines containing SP generate larger responses to flash photolysis of caged glutamate than SP-negative ones. An NMDA-receptor-mediated chemical long-term potentiation caused the accumulation of GFP-GluR1 in spine heads of control but not of shRNA-transfected, SP-deficient neurons. SP is linked to calcium stores, because their pharmacological blockade eliminated SP-related enhancement of glutamate responses, and release of calcium from stores produced an SP-dependent increase of GluR1 in spines. Thus, SP plays a crucial role in the calcium store-associated ability of neurons to undergo long-term plasticity.

show abstract

Section: Discussionmentioning

confidence: 98%

Synaptopodin Regulates Plasticity of Dendritic Spines in Hippocampal Neurons

Vlachos

Korkotian²,

Schonfeld³

et al. 2009

J. Neurosci.

171

217

View full text Add to dashboard Cite

show abstract

“…Brains were removed and post-fixed in the same fixative for a few hours at 4°C followed by cryoprotection in 20% sucrose in 0.1 M PB, pH 7.4, at 4°C overnight. Cryostat sections (40 m, coronal plane) of the hippocampus were processed for in situ hybridization as described previously (Deller et al, 2002).…”

Section: Materials and Methods Animals And Tissue Preparationmentioning

confidence: 99%

“…Although our previous electron microscopic studies had primarily revealed Synaptopodin in spines where it was associated with the spine apparatus, Synaptopodin immunoreactivity was also observed in the dendritic shafts of some neurons (Deller et al, 2000a(Deller et al, , 2002. Using three-dimensional confocal analysis (Figs.…”

Section: Cellular Distribution Of Synaptopodinpositive Structures In mentioning

confidence: 98%

“…1A-D), as previously described (Deller et al, 2002). Using high-magnification confocal laser scanning microscopy, Synaptopodin immunostaining was resolved into single immunofluorescent puncta, which could readily be distinguished.…”

Section: Synaptopodin Immunostaining In the Mouse Hippocampusmentioning

confidence: 99%

“…This pattern corresponds to the laminar organization of the hippocampus, which is generated by the layer-specific termination of extrinsic and intrinsic afferent fiber systems (Amaral and Witter, 1995). Of interest, the normal Synaptopodin distribution pattern is lost if the hippocampal cytoarchitecture is disrupted, for example, in reeler mice (Deller et al, 2002). On the basis of these data, we hypothesized that the immunolabeling pattern of Synaptopodin is generated by a layer-specific sorting of Synaptopodin along dendrites of hippocampal neurons (Deller et al, 2000a,b).…”

mentioning

confidence: 95%

See 2 more Smart Citations

Lamina‐specific distribution of synaptopodin, an actin‐associated molecule essential for the spine apparatus, in identified principal cell dendrites of the mouse hippocampus

Bas‐Orth

Vlachos

Turco

et al. 2005

J of Comparative Neurology

Self Cite

View full text Add to dashboard Cite

Synaptopodin is an actin-associated molecule found in a subset of telencephalic spines. It is an essential component of the spine apparatus, a Ca(2+)-storing organelle and has been implicated in synaptic plasticity (Deller et al. [2003] Proc Natl Acad Sci U S A 100:10494-10499). In the rodent hippocampus, Synaptopodin is distributed in a characteristic region- and lamina-specific manner. To learn more about the cellular basis underlying this distribution, the regional, laminar, and cellular localization of Synaptopodin and its mRNA were analyzed in mouse hippocampus. First, Synaptopodin puncta densities were quantified after immunofluorescent labeling using confocal microscopy. Second, the dendritic distribution of Synaptopodin-positive puncta was studied using three-dimensional confocal reconstructions of Synaptopodin-immunostained and enhanced green fluorescence protein (EGFP)-labeled principal neurons. Synaptopodin puncta located within dendrites of principal neurons were primarily found in spines (>95%). Analysis of dendritic segments located in different layers revealed lamina-specific differences in the percentage of Synaptopodin-positive spines. Densities ranged between 37% (outer molecular layer) and 14% (stratum oriens; CA1). Finally, synaptopodin mRNA expression was studied using in situ hybridization, laser microdissection, and quantitative reverse transcriptase-polymerase chain reaction. Expression levels were comparable between all regions. These data demonstrate a lamina-specific distribution of Synaptopodin within dendritic segments of identified neurons. Within dendrites, the majority of Synaptopodin-positive puncta were located in spines where they represent spine apparatuses. We conclude, that this organelle is distributed in a region- and layer-specific manner in the mouse hippocampus and suggest that differences in the activity of afferent fiber systems could determine its distribution.

show abstract

Loss of the cisternal organelle in the axon initial segment of cortical neurons in synaptopodin‐deficient mice

Bas‐Orth

Schultz

Müller

et al. 2007

J of Comparative Neurology

Self Cite

View full text Add to dashboard Cite

The axon initial segment of cortical neurons contains the so-called cisternal organelle, an enigmatic formation of stacked endoplasmic reticulum and interdigitating plates of electron-dense material. This organelle shows many structural similarities to the spine apparatus, a cellular organelle found in a subpopulation of dendritic spines. Whereas roles in calcium signaling and protein trafficking have been proposed for the spine apparatus, little is yet known about the physiological function of its putative axonal counterpart. Considering the structural similarity of these two organelles, we hypothesized that synaptopodin, a protein essential for the formation of the dendritic spine apparatus, could also be a component of the cisternal organelle. By using immunofluorescence microscopy, we found that synaptopodin is indeed located within the axon initial segments of principal neurons in the mouse neocortex and hippocampus. Pre-embedding immunogold labeling demonstrated a close association of synaptopodin immunoreactivity with the dense plates of cisternal organelles. In synaptopodin-deficient mice, ultrastructural analysis of identified axon initial segments of CA1 pyramidal cells revealed a lack of cisternal organelles similar to the reported lack of spine apparatuses in these mutants. However, in vitro patch clamp recording of mutant neurons showed that the lack of cisternal organelles did not lead to any changes in basic electrophysiological parameters of action potentials. Taken together, our data demonstrate that synaptopodin is an essential component of the cisternal organelle of axons and of the dendritic spine apparatus, two organelles that are structurally and molecularly related.

show abstract

Laminar distribution of synaptopodin in normal and reeler mouse brain depends on the position of spine‐bearing neurons

Cited by 14 publications

References 41 publications

Synaptopodin Regulates Plasticity of Dendritic Spines in Hippocampal Neurons

Synaptopodin Regulates Plasticity of Dendritic Spines in Hippocampal Neurons

Lamina‐specific distribution of synaptopodin, an actin‐associated molecule essential for the spine apparatus, in identified principal cell dendrites of the mouse hippocampus

Loss of the cisternal organelle in the axon initial segment of cortical neurons in synaptopodin‐deficient mice

Contact Info

Product

Resources

About