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The class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus.

Proper circuit function in the mammalian nervous system depends on the precise assembly and development of excitatory and inhibitory synaptic connections between neurons. Through a loss-of-function genetic screen in cultured hippocampal neurons, we previously identified the class 4 Semaphorin Sema4D... Full description

Journal Title: The Journal of neuroscience : the official journal of the Society for Neuroscience May 22, 2013, Vol.33(21), pp.8961-8973
Main Author: Kuzirian, Marissa S
Other Authors: Moore, Anna R , Staudenmaier, Emily K , Friedel, Roland H , Paradis, Suzanne
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: E-ISSN: 1529-2401 ; DOI: 10.1523/JNEUROSCI.0989-13.2013
Link: http://search.proquest.com/docview/1355475875/?pq-origsite=primo
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title: The class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus.
format: Article
creator:
  • Kuzirian, Marissa S
  • Moore, Anna R
  • Staudenmaier, Emily K
  • Friedel, Roland H
  • Paradis, Suzanne
subjects:
  • Analysis of Variance–Chemistry
  • Animals–Pharmacology
  • Animals, Newborn–Cytology
  • Antigens, CD–Physiology
  • Cells, Cultured–Drug Effects
  • Cerebral Cortex–Metabolism
  • Embryo, Mammalian–Genetics
  • Female–Metabolism
  • Gabaergic Neurons–Drug Effects
  • Gene Expression Regulation–Cytology
  • Glutamate Decarboxylase–Pharmacology
  • Green Fluorescent Proteins–Metabolism
  • Growth Cones–Metabolism
  • Hippocampus–Chemistry
  • Immunoglobulin Fc Fragments–Pharmacology
  • Male–Pharmacology
  • Mice–Physiology
  • Nerve Tissue Proteins–Drug Effects
  • Organ Culture Techniques–Genetics
  • Patch-Clamp Techniques–Pharmacology
  • Rats–Pharmacology
  • Receptors, Gaba-A–Pharmacology
  • Semaphorins–Pharmacology
  • Sodium Channel Blockers–Pharmacology
  • Synapses–Pharmacology
  • Synaptic Potentials–Pharmacology
  • Tetrodotoxin–Pharmacology
  • Time Factors–Pharmacology
  • Antigens, CD
  • Cd100 Antigen
  • Immunoglobulin Fc Fragments
  • Nerve Tissue Proteins
  • Receptors, Gaba-A
  • Semaphorins
  • Sodium Channel Blockers
  • Green Fluorescent Proteins
  • Tetrodotoxin
  • Glutamate Decarboxylase
  • Glutamate Decarboxylase 2
ispartof: The Journal of neuroscience : the official journal of the Society for Neuroscience, May 22, 2013, Vol.33(21), pp.8961-8973
description: Proper circuit function in the mammalian nervous system depends on the precise assembly and development of excitatory and inhibitory synaptic connections between neurons. Through a loss-of-function genetic screen in cultured hippocampal neurons, we previously identified the class 4 Semaphorin Sema4D as being required for proper GABAergic synapse development. Here we demonstrate that Sema4D is sufficient to promote GABAergic synapse formation in rodent hippocampus and investigate the kinetics of this activity. We find that Sema4D treatment of rat hippocampal neurons increases the density of GABAergic synapses as detected by immunocytochemistry within 30 min, much more rapidly than has been previously described for a prosynaptogenic molecule, and show that this effect is dependent on the Sema4D receptor PlexinB1 using PlxnB1(-/-) mice. Live imaging studies reveal that Sema4D elicits a rapid enhancement (within 10 min) in the rate of addition of synaptic proteins. Therefore, we demonstrate that Sema4D, via PlexinB1, acts to initiate synapse formation by recruiting molecules to both the presynaptic and the postsynaptic terminals; these nascent synapses subsequently become fully functional by 2 h after Sema4D treatment. In addition, acute treatment of an organotypic hippocampal slice epilepsy model with Sema4D reveals that Sema4D rapidly and dramatically alters epileptiform activity, which is consistent with a Sema4D-mediated shift in the balance of excitation and inhibition within the circuit. These data demonstrate an ability to quickly assemble GABAergic synapses in response to an appropriate signal and suggest a potential area of exploration for the development of novel antiepileptic drugs.
language: eng
source:
identifier: E-ISSN: 1529-2401 ; DOI: 10.1523/JNEUROSCI.0989-13.2013
fulltext: fulltext
issn:
  • 15292401
  • 1529-2401
url: Link


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titleThe class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus.
creatorKuzirian, Marissa S ; Moore, Anna R ; Staudenmaier, Emily K ; Friedel, Roland H ; Paradis, Suzanne
contributorKuzirian, Marissa S (correspondence author) ; Kuzirian, Marissa S (record owner)
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identifierE-ISSN: 1529-2401 ; DOI: 10.1523/JNEUROSCI.0989-13.2013
subjectAnalysis of Variance–Chemistry ; Animals–Pharmacology ; Animals, Newborn–Cytology ; Antigens, CD–Physiology ; Cells, Cultured–Drug Effects ; Cerebral Cortex–Metabolism ; Embryo, Mammalian–Genetics ; Female–Metabolism ; Gabaergic Neurons–Drug Effects ; Gene Expression Regulation–Cytology ; Glutamate Decarboxylase–Pharmacology ; Green Fluorescent Proteins–Metabolism ; Growth Cones–Metabolism ; Hippocampus–Chemistry ; Immunoglobulin Fc Fragments–Pharmacology ; Male–Pharmacology ; Mice–Physiology ; Nerve Tissue Proteins–Drug Effects ; Organ Culture Techniques–Genetics ; Patch-Clamp Techniques–Pharmacology ; Rats–Pharmacology ; Receptors, Gaba-A–Pharmacology ; Semaphorins–Pharmacology ; Sodium Channel Blockers–Pharmacology ; Synapses–Pharmacology ; Synaptic Potentials–Pharmacology ; Tetrodotoxin–Pharmacology ; Time Factors–Pharmacology ; Antigens, CD ; Cd100 Antigen ; Immunoglobulin Fc Fragments ; Nerve Tissue Proteins ; Receptors, Gaba-A ; Semaphorins ; Sodium Channel Blockers ; Green Fluorescent Proteins ; Tetrodotoxin ; Glutamate Decarboxylase ; Glutamate Decarboxylase 2
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descriptionProper circuit function in the mammalian nervous system depends on the precise assembly and development of excitatory and inhibitory synaptic connections between neurons. Through a loss-of-function genetic screen in cultured hippocampal neurons, we previously identified the class 4 Semaphorin Sema4D as being required for proper GABAergic synapse development. Here we demonstrate that Sema4D is sufficient to promote GABAergic synapse formation in rodent hippocampus and investigate the kinetics of this activity. We find that Sema4D treatment of rat hippocampal neurons increases the density of GABAergic synapses as detected by immunocytochemistry within 30 min, much more rapidly than has been previously described for a prosynaptogenic molecule, and show that this effect is dependent on the Sema4D receptor PlexinB1 using PlxnB1(-/-) mice. Live imaging studies reveal that Sema4D elicits a rapid enhancement (within 10 min) in the rate of addition of synaptic proteins. Therefore, we demonstrate that Sema4D, via PlexinB1, acts to initiate synapse formation by recruiting molecules to both the presynaptic and the postsynaptic terminals; these nascent synapses subsequently become fully functional by 2 h after Sema4D treatment. In addition, acute treatment of an organotypic hippocampal slice epilepsy model with Sema4D reveals that Sema4D rapidly and dramatically alters epileptiform activity, which is consistent with a Sema4D-mediated shift in the balance of excitation and inhibition within the circuit. These data demonstrate an ability to quickly assemble GABAergic synapses in response to an appropriate signal and suggest a potential area of exploration for the development of novel antiepileptic drugs.
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10Glutamate Decarboxylase–Pharmacology
11Green Fluorescent Proteins–Metabolism
12Growth Cones–Metabolism
13Hippocampus–Chemistry
14Immunoglobulin Fc Fragments–Pharmacology
15Male–Pharmacology
16Mice–Physiology
17Nerve Tissue Proteins–Drug Effects
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23Sodium Channel Blockers–Pharmacology
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25Synaptic Potentials–Pharmacology
26Tetrodotoxin–Pharmacology
27Time Factors–Pharmacology
28Antigens, CD
29Cd100 Antigen
30Immunoglobulin Fc Fragments
31Nerve Tissue Proteins
32Receptors, Gaba-A
33Semaphorins
34Sodium Channel Blockers
35Green Fluorescent Proteins
36Tetrodotoxin
37Glutamate Decarboxylase
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titleThe class 4 semaphorin Sema4D promotes the rapid assembly of GABAergic synapses in rodent hippocampus.
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5Cerebral Cortex–Metabolism
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7Female–Metabolism
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10Glutamate Decarboxylase–Pharmacology
11Green Fluorescent Proteins–Metabolism
12Growth Cones–Metabolism
13Hippocampus–Chemistry
14Immunoglobulin Fc Fragments–Pharmacology
15Male–Pharmacology
16Mice–Physiology
17Nerve Tissue Proteins–Drug Effects
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19Patch-Clamp Techniques–Pharmacology
20Rats–Pharmacology
21Receptors, Gaba-A–Pharmacology
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