In vivo clonal overexpression of neuroligin 3 and neuroligin 2 in neurons of the rat cerebral cortex: Differential effects on GABAergic synapses and neuronal migration

We studied the effect of clonal overexpression of neuroligin 3 (NL3) or neuroligin 2 (NL2) in the adult rat cerebral cortex following in utero electroporation (IUEP) at embryonic stage E14. Overexpression of NL3 leads to a large increase in vesicular gamma‐aminobutyric acid (GABA) transporter (vGAT)...

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Published in:Journal of comparative neurology (1911) 2015-06, Vol.523 (9), p.1359-1378
Main Authors: Fekete, Christopher D., Chiou, Tzu-Ting, Miralles, Celia P., Harris, Rachel S., Fiondella, Christopher G., Loturco, Joseph J., De Blas, Angel L.
Format: Article
Language:English
Subjects:
Adjuvants, Immunologic
Animals
Cell Adhesion Molecules, Neuronal - genetics
Cell Adhesion Molecules, Neuronal - metabolism
Cell Movement - physiology
Cells, Cultured
Cerebral Cortex - metabolism
Electroporation
gamma-Aminobutyric Acid - metabolism
gephyrin
Glutamate Decarboxylase - metabolism
glutamic acid decarboxylase
in utero electroporation
Membrane Proteins - genetics
Membrane Proteins - metabolism
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
neuronal migration
Neurons - metabolism
Parvalbumins - metabolism
Rats, Sprague-Dawley
Rats, Wistar
synapse formation
Synapses - metabolism
Transfection
vesicular GABA transporter
Vesicular Glutamate Transport Protein 1 - metabolism
Vesicular Inhibitory Amino Acid Transport Proteins - metabolism
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Summary:We studied the effect of clonal overexpression of neuroligin 3 (NL3) or neuroligin 2 (NL2) in the adult rat cerebral cortex following in utero electroporation (IUEP) at embryonic stage E14. Overexpression of NL3 leads to a large increase in vesicular gamma‐aminobutyric acid (GABA) transporter (vGAT) and glutamic acid decarboxylase (GAD)65 in the GABAergic contacts that the overexpressing neurons receive. Overexpression of NL2 produced a similar effect but to a lesser extent. In contrast, overexpression of NL3 or NL2 after IUEP does not affect vesicular glutamate transporter 1 (vGlut1) in the glutamatergic contacts that the NL3 or NL2‐overexpressing neurons receive. The NL3 or NL2‐overexpressing neurons do not show increased innervation by parvalbumin‐containing GABAergic terminals or increased parvalbumin in the same terminals that show increased vGAT. These results indicate that the observed increase in vGAT and GAD65 is not due to increased GABAergic innervation but to increased expression of vGAT and GAD65 in the GABAergic contacts that NL3 or NL2‐overexpressing neurons receive. The majority of bright vGAT puncta contacting the NL3‐overexpressing neurons have no gephyrin juxtaposed to them, indicating that many of these contacts are nonsynaptic. This contrasts with the majority of the NL2‐overexpressing neurons, which show plenty of synaptic gephyrin clusters juxtaposed to vGAT. Besides having an effect on GABAergic contacts, overexpression of NL3 interferes with the neuronal radial migration, in the cerebral cortex, of the neurons overexpressing NL3. J. Comp. Neurol. 523:1359–1378, 2015. © 2015 Wiley Periodicals, Inc. Using in utero electroporation for overexpression of neuroligin 3 or neuroligin 2, the authors show that the neurons of the cerebral cortex overexpressing these neuroligins receive synaptic and non‐synaptic GABAergic contacts in which vGAT and GAD65 are highly increased J. Comp. Neurol., 2015.
ISSN:0021-9967
1096-9861
DOI:10.1002/cne.23740