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Although the regulation of neuronal excitability by phosphorylation of voltage-gated channels is widespread, the neuromodulation of ligand-gated channels, crucial for the control of synaptic strength, has been reported in only a few instances []. Because the modification of synaptic strength through the action of second-messenger systems should be an effective way to regulate the computational capabilities of neuronal circuits, this form of neuromodulation could be as common as the ones that affect electrical excitability. We anticipated that the hippocampus might be a favorable site to search for synaptic neuromodulation; this brain region is well known to regulate synaptic strength by long-term potentiation [7], and the abundantly represented glutamate receptor channels in hippocampus have been implicated in memory, epilepsy, excitotoxicity, and some neurodegenerative diseases [8]. We used both the whole-cell recording and the outside-out mode of the standard patch-clamp method [9] to study responses to glutamate in 2- to 7-day-old cultured hippocampal pyramidal neurons from newborn Long Evans rats [10]. We included 5 [micrometer] magnesium adenosine trisphosphate MgATP in all the whole-cell recordings to prevent "run-down" of glutamate-induced responses [11]. Because adenylate cyclase is commonly involved in neuromodulatory systems, we examined responses to glutamate in whole-cell recordings before and after treatment with forskolin FSK , an activator of adenylate cyclase [12].

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Synaptic cell adhesion molecules represent important targets for neuronal activity-dependent proteolysis. Postsynaptic neuroligins NLs form trans-synaptic complexes with presynaptic neurexins NXs. Both NXs and NLs are cleaved from the cell surface by metalloproteases in an activity-dependent manner, releasing a soluble extracellular fragment and membrane-tethered C-terminal fragment.

The cleavage of NL1 depresses synaptic transmission, but the mechanism by which this occurs is unknown. Metabotropic glutamate receptor 2 mGluR2 are located primarily at the periphery of presynaptic terminals, where they inhibit the formation of cyclic adenosine monophosphate cAMP and consequently suppress the release of glutamate and decrease synaptic transmission. In the present study, we found that the soluble ectodomain of NL1 binds to and activates mGluR2 in both neurons and heterologous cells, resulting in a decrease in cAMP formation.

In a slice preparation from the hippocampus of mice, NL1 inhibited the release of glutamate from mossy fibers that project to CA3 pyramidal neurons. The presynaptic effect of NL1 was abolished in the presence of a selective antagonist for mGluR2. Thus, our data suggest that the soluble extracellular domain of NL1 functionally interacts with mGluR2 and thereby decreases synaptic strength. The development and function of neuronal synapses depend on bidirectional interactions between pre- and postsynaptic components Sanes and Lichtman, Deletions of human NX genes might be involved in the pathology of schizophrenia whereas NL gene mutations are indicated in schizophrenia Zhang Z.

NLs are essential for synaptic functions and alterations in their expression can lead to deficits in memory formation and synaptic plasticity Zhang B. For example, the overexpression of NL1 shifts synaptic activity toward greater excitation, resulting in impairment in the induction of long-term potentiation LTP and deficits in memory acquisition Dahlhaus et al. Interestingly, global NL1 depletion also leads to impairments in hippocampal LTP and deficits in spatial learning and memory Blundell et al.

The acute suppression of NL1 in the amygdala prevents the induction of LTP and results in deficits in the storage of associative fear memory Kim et al. Neuronal activity can induce the cleavage of both NX and NL from their pre- and postsynaptic membranes Bot et al. In addition, accumulation of the soluble extracellular fragment of NL1 leads to a decrease in neurotransmitter release from excitatory synapses Peixoto et al.

Based on these results, we hypothesized that the cleaved fraction of NL1 activates presynaptic receptors that inhibit transmitter release. At excitatory synapses metabotropic receptors for glutamate mGluRs regulate presynaptic glutamate release and modify postsynaptic excitability to glutamate reviewed by Niswender and Conn, Group I receptors mGluR1 and mGluR5 are mainly located postsynaptically where they induce inositol phospholipid hydrolysis.

Their activation increases neuronal excitability Niswender and Conn, They are coupled to G i proteins that, when activated, prevent the formation of cyclic adenosine monophosphate cAMP , thereby decreasing the release of glutamate Niswender and Conn, In the hippocampus, this pathway inhibits the release of glutamate from mossy fibers that project to CA3 pyramidal neurons.

Hippocampal neurons were obtained on embryonic day 18—19 from Wistar rat embryos Charles River Laboratories, Kisselegg, Germany as described previously Owczarek et al.

Briefly, the hippocampi were dissected, cleared from blood vessels and meninges, mechanically chopped and trypsinized. The animals were treated in accordance with the Danish Animal Welfare Act, and the study was approved by the Department of Experimental Medicine at the University of Copenhagen. Hippocampal neurons were grown for 7 days. Additionally, tetrodotoxin TTX was used to avoid the indirect effect on cAMP production that could be mediated by cell depolarization Prezeau et al.

In some experiments, non-competitive mGluR2 inhibitor RO was used. Forty-eight hours after transfection, the cells were lysed in IP buffer supplemented with complete protease inhibitors Roche Diagnostics , and cleared lysates were incubated with appropriate antibody overnight. The surgical procedures complied with Danish legislation. This study was carried out in accordance with the recommendations of Department of Experimental Medicine of the University of Copenhagen. The protocol was approved by the Department of Experimental Medicine of the University of Copenhagen.

Measurements were performed at room temperature in a recording chamber that was perfused with oxygenated aCSF. The pipette solution contained mM K-gluconate, 2. The stimulus intensity was set between 0. The stimulation consisted of a pair of shocks that were applied at 50— ms intervals. The effects of NL1 on synaptic transmission were tested by puff-applying ecto-NL1 4. The puff lasted ms and ended 10 ms before the electrical stimulation.

Following tests were used: paired and unpaired t -test for normally distributed dataset. The data were analyzed using GraphPad Prism 6 software. High neuronal activity results in the intensive shedding of NL1 from the postsynaptic membrane Peixoto et al. The accumulation of this soluble extracellular fragment leads to a decrease in synaptic activity Peixoto et al. We investigated the mechanism responsible for this process. One possibility is that cleaved NLs interact with presynaptic receptors and thereby regulate neurotransmitter release.

We first tested whether the soluble NL1 affects the formation of cAMP in hippocampal primary neuronal cultures. We induced the formation of cAMP with forskolin Kingston et al. Indeed, in the presence of RO , NL1 Next, we tested whether ecto-NL1 activates mGluR2 in heterologous cells.

Additionally, we performed a similar experiment with mGluR3 but did not observe any change induced by ecto-NL1 in cAMP level data not shown. We therefore focused on mGluR2. Figure 1. Soluble neuroligin 1 NL1 ectodomain reduces cyclic adenosine monophosphate cAMP levels via activation of metabotropic glutamate receptor 2 mGluR2.

Glutamate was used as a positive control. The cleavage of NL1 decreases the release of glutamate Peixoto et al. We reasoned that the extracellular portion of NL1 might appear in close proximity to the presynaptic membrane, thus allowing a direct interaction with mGluRs.

To test this hypothesis, we performed pull-down experiments from P4—5 rat brain extracts. Importantly, immunoreactivity from NL1 clearly showed two bands with molecular weights around and 90 kDa, respectively, corresponding to the full-length and extracellular domain of NL1 Peixoto et al. This observation confirms that the NL1 ectodomain interacts with mGluR2. Figure 2. NL1 interacts with mGluR2.

Goat normal serum was used as a negative control IgG. Immunoblots for NL1 also yielded two bands for full-length protein kDa and a soluble ectodomain around 90 kDa. Protein complexes were immunoprecipitated IP and probed WB with the indicated antibodies. Mouse IgG was used as a negative control. All HA-blots come from the same membrane. Bands at and 90 kDa represent HA-NL1 full length and soluble ectodomain, respectively, and bands at and kDa represent mGluR2 monomer and dimer, respectively.

HA-blots come from the same membrane. Bands at and kDa represent mGluR2 monomer and dimer, respectively. Ecto-NL1 was previously shown to decrease synaptic activity in dissociated hippocampal neurons Peixoto et al.

To confirm these results in a slice preparation from the mouse brain, we stimulated mossy fiber-CA3 synapses known to express mGluR2 at preterminal levels Yokoi et al. We recorded pyramidal neurons from the CA3 region by means of the whole-cell patch-clamp technique. Altogether, our data demonstrate that ecto-NL1 induced presynaptic inhibition of the mossy fiber-CA3 synapse.

Figure 3. The NL1 ectodomain produces presynaptic inhibition in CA3 neurons. A Schematic diagram of the preparation. The synaptic stimulation of mossy fibers was produced by a bipolar electrode red , patch electrode black , and focal puff application of ecto-NL1 green. B—E Response of a CA3 neuron to two stimulations S1 and S2 under control conditions black and after puffing ecto-NL1 near the apical dendrite of the recorded neuron green.

In F—H bars show the mean values and lines correspond to individual pairs of values. Figure 4. Five superimposed recordings. B Recording from the same neuron after a single puff of ecto-NL1 near the apical dendrite of the recorded neuron five superimposed traces. Note the strong decrease in the frequency of mEPSCs. Significant decrease mean frequency of mEPSCs in control conditions: 1.

Bars show the mean values and lines correspond to individual pairs of values. In spite of the lack of significant decrease of synaptic transmission, the PPR was increased from 1. Altogether these results show that at least part of the presynaptic inhibition induced by ecto-NL1 was caused by the activation of mGluR2.

Figure 5. RO reduces the presynaptic inhibitory effect of NL1. B—D Response of a CA3 neuron to two stimulations S1 and S2 under control conditions iron and after puffing ecto-NL1 near the apical dendrite of the recorded neuron teal. D The PPR was slightly decreased from 1. G Significant increase for the PPR for all cells together from 1.

In E—G bars show the mean values and lines correspond to individual pairs of values. Figure 6. No significant decrease mean frequency of mEPSCs in control conditions: 0. No significant change mean amplitude of mEPSCs in control conditions: Our data suggest that the extracellular soluble fragment of NL1 ecto-NL1 decreases glutamatergic synaptic transmission by binding to and activating presynaptic mGluR2. This activation prevents the formation of cAMP, which in turn suppresses the release of glutamate Niswender and Conn, , eventually decreasing synaptic strength.

Three arguments support this interpretation.

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Synaptic cell adhesion molecules represent important targets for neuronal activity-dependent proteolysis. Postsynaptic neuroligins NLs form trans-synaptic complexes with presynaptic neurexins NXs. Both NXs and NLs are cleaved from the cell surface by metalloproteases in an activity-dependent manner, releasing a soluble extracellular fragment and membrane-tethered C-terminal fragment. The cleavage of NL1 depresses synaptic transmission, but the mechanism by which this occurs is unknown. Metabotropic glutamate receptor 2 mGluR2 are located primarily at the periphery of presynaptic terminals, where they inhibit the formation of cyclic adenosine monophosphate cAMP and consequently suppress the release of glutamate and decrease synaptic transmission. In the present study, we found that the soluble ectodomain of NL1 binds to and activates mGluR2 in both neurons and heterologous cells, resulting in a decrease in cAMP formation. In a slice preparation from the hippocampus of mice, NL1 inhibited the release of glutamate from mossy fibers that project to CA3 pyramidal neurons. The presynaptic effect of NL1 was abolished in the presence of a selective antagonist for mGluR2.

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