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Different changes in pre- and postsynaptic components in the hippocampal CA1 subfield after transient global cerebral ischemia

Abstract

To date, ischemia-induced damage to dendritic spines has attracted considerable attention, while the possible effects of ischemia on presynaptic components has received relatively less attention. To further examine ischemia-induced changes in pre- and postsynaptic specializations in the hippocampal CA1 subfield, we modeled global cerebral ischemia with two-stage 4-vessel-occlusion in rats, and found that three postsynaptic markers, microtubule-associated protein 2 (MAP2), postsynaptic density protein 95 (PSD95), and filamentous F-actin (F-actin), were all substantially decreased in the CA1 subfield after ischemia/reperfusion (I/R). Although no significant change was detected in synapsin I, a presynaptic marker, in the CA1 subfield at the protein level, confocal microscopy revealed that the number and size of synapsin I puncta were significantly changed in the CA1 stratum radiatum after I/R. The size of synapsin I puncta became slightly, but significantly reduced on Day 1.5 after I/R. From Days 2 to 7 after I/R, the number of synapsin I puncta became moderately decreased, while the size of synapsin I puncta was significantly increased. Interestingly, some enlarged puncta of synapsin I were observed in close proximity to the dendritic shafts of CA1 pyramidal cells. Due to the more substantial decrease in the number of F-actin puncta, the ratio of synapsin I/F-actin puncta was significantly increased after I/R. The decrease in synapsin I puncta size in the early stage of I/R may be the result of excessive neurotransmitter release due to I/R-induced hyperexcitability in CA3 pyramidal cells, while the increase in synapsin I puncta in the later stage of I/R may reflect a disability of synaptic vesicle release due to the loss of postsynaptic contacts.

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Abbreviations

CNS:

Central nervous system

DG:

Dentate gyrus

F-actin:

Filamentous actin

F/G:

F-actin/G-actin

G-actin:

Globular monomeric form of actin

GAPDH:

Glyceraldehyde-3-phosphate dehydrogenase

HF:

Hippocampal fissure

Ig:

Immunoglobulin

I/R:

Ischemia/reperfusion

MAP2:

Microtubule-associated protein 2

PB:

Phosphate buffer

PSD:

Postsynaptic density protein

PSD95:

Postsynaptic density protein 95

SL:

Stratum lucidum

SNAP-25:

Synaptosomal-associated protein 25

SVP-38:

Synaptic vesicle-associated protein 38

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Funding

This work was supported by National Natural Science Foundation of China (General Program), grant number: 81871014 (to YC Li).

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Authors

Contributions

YZ and BHT equally contributed to this work: investigation, validation, and writing. YCL conceived and designed the study. SW and CHW: software, formal analysis, writing. JLS and YG: software, formal analysis. All authors critically reviewed and approved the final version of the paper.

Corresponding author

Correspondence to Yan-Chao Li.

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Conflict of interest

The author declared no conflict of interest.

Ethics approval

The experimental procedures adhered to the ethical principles of experiments on animals of Jilin University, and were approved by the Animal Research Committee of Jilin University (Permit Number: SYXK(Ji) 2017–0003).

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Zhang, Y., Tan, BH., Wu, S. et al. Different changes in pre- and postsynaptic components in the hippocampal CA1 subfield after transient global cerebral ischemia. Brain Struct Funct 227, 345–360 (2022). https://doi.org/10.1007/s00429-021-02404-7

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  • DOI: https://doi.org/10.1007/s00429-021-02404-7

Keywords

  • Dendritic spine
  • F-actin, synapsin I
  • Transient cerebral ischemia
  • Rat
  • CA1 pyramidal neuron