Differential involvement of perineuronal astrocytes and microglia in synaptic stripping after hypoglossal axotomy

Jun Yamada, Hiroshi Nakanishi, Shozo Jinno

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Following peripheral axotomy, the presynaptic terminals are removed from lesioned neurons, that is synaptic stripping. To elucidate involvement of astrocytes and microglia in synaptic stripping, we herein examined the motoneuron perineuronal circumference after hypoglossal nerve transection. As reported previously, axotomy-induced slow cell death occurred in C57BL/6 mice but not in Wistar rats. Synaptophysin labeling in the hypoglossal nucleus exhibited a minor reduction in both species after axotomy. Slice patch recording showed that the mean frequency of miniature postsynaptic currents in axotomized motoneurons was significantly lower in rats than in mice. We then estimated the relative coverage of motoneuron perineuronal circumference by line profile analysis. In the synaptic environment, axotomy-induced intrusion of astrocytic processes was significantly more extensive in rats than in mice, whereas microglial intrusion into the synaptic space was significantly more severe in mice than in rats. Interestingly, in the extrasynaptic environment, the prevalence of contact between astrocytic processes and lesioned motoneurons was significantly increased in rats, while no significant axotomy-induced alterations in astrocytic contact were observed in mice. These findings indicate that astrocytic, but not microglial, reaction may primarily mediate some anti-apoptotic effects through synaptic stripping after hypoglossal nerve axotomy. In addition, enlargement of astrocytic processes in the extrasynaptic environment may also be involved in neuronal protection via the increased uptake of excessive glutamate.

Original languageEnglish
Pages (from-to)1-10
Number of pages10
JournalNeuroscience
Volume182
DOIs
Publication statusPublished - May 19 2011

Fingerprint

Axotomy
Microglia
Astrocytes
Motor Neurons
Hypoglossal Nerve Injuries
Hypoglossal Nerve
Synaptic Potentials
Synaptophysin
Presynaptic Terminals
Inbred C57BL Mouse
Wistar Rats
Glutamic Acid
Cell Death
Neurons

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

Differential involvement of perineuronal astrocytes and microglia in synaptic stripping after hypoglossal axotomy. / Yamada, Jun; Nakanishi, Hiroshi; Jinno, Shozo.

In: Neuroscience, Vol. 182, 19.05.2011, p. 1-10.

Research output: Contribution to journalArticle

@article{c6f1ae9136c04394a1470a5dfe47040c,
title = "Differential involvement of perineuronal astrocytes and microglia in synaptic stripping after hypoglossal axotomy",
abstract = "Following peripheral axotomy, the presynaptic terminals are removed from lesioned neurons, that is synaptic stripping. To elucidate involvement of astrocytes and microglia in synaptic stripping, we herein examined the motoneuron perineuronal circumference after hypoglossal nerve transection. As reported previously, axotomy-induced slow cell death occurred in C57BL/6 mice but not in Wistar rats. Synaptophysin labeling in the hypoglossal nucleus exhibited a minor reduction in both species after axotomy. Slice patch recording showed that the mean frequency of miniature postsynaptic currents in axotomized motoneurons was significantly lower in rats than in mice. We then estimated the relative coverage of motoneuron perineuronal circumference by line profile analysis. In the synaptic environment, axotomy-induced intrusion of astrocytic processes was significantly more extensive in rats than in mice, whereas microglial intrusion into the synaptic space was significantly more severe in mice than in rats. Interestingly, in the extrasynaptic environment, the prevalence of contact between astrocytic processes and lesioned motoneurons was significantly increased in rats, while no significant axotomy-induced alterations in astrocytic contact were observed in mice. These findings indicate that astrocytic, but not microglial, reaction may primarily mediate some anti-apoptotic effects through synaptic stripping after hypoglossal nerve axotomy. In addition, enlargement of astrocytic processes in the extrasynaptic environment may also be involved in neuronal protection via the increased uptake of excessive glutamate.",
author = "Jun Yamada and Hiroshi Nakanishi and Shozo Jinno",
year = "2011",
month = "5",
day = "19",
doi = "10.1016/j.neuroscience.2011.03.030",
language = "English",
volume = "182",
pages = "1--10",
journal = "Neuroscience",
issn = "0306-4522",
publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Differential involvement of perineuronal astrocytes and microglia in synaptic stripping after hypoglossal axotomy

AU - Yamada, Jun

AU - Nakanishi, Hiroshi

AU - Jinno, Shozo

PY - 2011/5/19

Y1 - 2011/5/19

N2 - Following peripheral axotomy, the presynaptic terminals are removed from lesioned neurons, that is synaptic stripping. To elucidate involvement of astrocytes and microglia in synaptic stripping, we herein examined the motoneuron perineuronal circumference after hypoglossal nerve transection. As reported previously, axotomy-induced slow cell death occurred in C57BL/6 mice but not in Wistar rats. Synaptophysin labeling in the hypoglossal nucleus exhibited a minor reduction in both species after axotomy. Slice patch recording showed that the mean frequency of miniature postsynaptic currents in axotomized motoneurons was significantly lower in rats than in mice. We then estimated the relative coverage of motoneuron perineuronal circumference by line profile analysis. In the synaptic environment, axotomy-induced intrusion of astrocytic processes was significantly more extensive in rats than in mice, whereas microglial intrusion into the synaptic space was significantly more severe in mice than in rats. Interestingly, in the extrasynaptic environment, the prevalence of contact between astrocytic processes and lesioned motoneurons was significantly increased in rats, while no significant axotomy-induced alterations in astrocytic contact were observed in mice. These findings indicate that astrocytic, but not microglial, reaction may primarily mediate some anti-apoptotic effects through synaptic stripping after hypoglossal nerve axotomy. In addition, enlargement of astrocytic processes in the extrasynaptic environment may also be involved in neuronal protection via the increased uptake of excessive glutamate.

AB - Following peripheral axotomy, the presynaptic terminals are removed from lesioned neurons, that is synaptic stripping. To elucidate involvement of astrocytes and microglia in synaptic stripping, we herein examined the motoneuron perineuronal circumference after hypoglossal nerve transection. As reported previously, axotomy-induced slow cell death occurred in C57BL/6 mice but not in Wistar rats. Synaptophysin labeling in the hypoglossal nucleus exhibited a minor reduction in both species after axotomy. Slice patch recording showed that the mean frequency of miniature postsynaptic currents in axotomized motoneurons was significantly lower in rats than in mice. We then estimated the relative coverage of motoneuron perineuronal circumference by line profile analysis. In the synaptic environment, axotomy-induced intrusion of astrocytic processes was significantly more extensive in rats than in mice, whereas microglial intrusion into the synaptic space was significantly more severe in mice than in rats. Interestingly, in the extrasynaptic environment, the prevalence of contact between astrocytic processes and lesioned motoneurons was significantly increased in rats, while no significant axotomy-induced alterations in astrocytic contact were observed in mice. These findings indicate that astrocytic, but not microglial, reaction may primarily mediate some anti-apoptotic effects through synaptic stripping after hypoglossal nerve axotomy. In addition, enlargement of astrocytic processes in the extrasynaptic environment may also be involved in neuronal protection via the increased uptake of excessive glutamate.

UR - http://www.scopus.com/inward/record.url?scp=79955482517&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=79955482517&partnerID=8YFLogxK

U2 - 10.1016/j.neuroscience.2011.03.030

DO - 10.1016/j.neuroscience.2011.03.030

M3 - Article

C2 - 21435379

AN - SCOPUS:79955482517

VL - 182

SP - 1

EP - 10

JO - Neuroscience

JF - Neuroscience

SN - 0306-4522

ER -