A novel role for cyclic guanosine 3′,5′monophosphate signaling in synaptic plasticity: A selective suppressor of protein kinase A-dependent forms of long-term potentiation

Makhinson, Michael; Opazo, Patricio; Carlisle, Holly J.; Godsil, Bill P.; Grant, Seth G. N.; O’Dell, Thomas J.

doi:10.1016/j.neuroscience.2006.02.018

Cited by 16 publications

(19 citation statements)

References 59 publications

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“…In addition, baseline synaptic responses were also not altered in cells infused with 8-Br-cAMP (Fig. 5C) (N ϭ 7), consistent with previous studies (Blitzer et al, 1995;Makhinson et al, 2006). To test whether TBP-induced LTP or the associated spine expansion are affected by previous activation of postsynaptic PKA, we loaded pyramidal cells with 8-Br-cAMP for 15-20 min, and then applied TBP.…”

Section: Spine Expansion Occurs But Does Not Persist Under Conditionssupporting

confidence: 87%

“…7D) (140 Ϯ 15%; N ϭ 54 spines/6 cells; p ϭ 0.95 compared with control spine expansion). It has been suggested that PP1 can be endogenously inactivated by PKA (Kang-Park et al, 2003;Makhinson et al, 2006), and so we would anticipate that persistently elevated PKA activity in the postsynaptic cell would have an effect similar to that of okadaic acid. We tested this possibility by including 8-Br-cAMP in the recording pipette solution, and we repeated the above experiments using LFS.…”

Section: Spine Stabilization and Ltp Consolidation Are Both Disruptedmentioning

confidence: 99%

“…Within this time window, LTP can be depotentiated by low-frequency activity (LFS), through a mechanism that requires PP1 (O'Dell et al, 1994;Zhou et al, 2003). PKA can prevent depotentiation by leading to phosphorylation of inhibitor 1, which in turn inhibits PP1 (Kang-Park et al, 2003;Makhinson et al, 2006). To determine whether the consolidation of spine expansion is subject to reversal through mechanisms that are similar to those involved in depotentiation, we examined whether spine expansion is subject to activity-dependent reversal, and if so, whether the same mechanisms are involved in this reversal of spine expansion as in synaptic depotentiation.…”

Section: Spine Stabilization and Ltp Consolidation Are Both Disruptedmentioning

confidence: 99%

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Spine Expansion and Stabilization Associated with Long-Term Potentiation

Yang¹,

Wang²,

Frerking³

et al. 2008

J. Neurosci.

188

248

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Stable expression of long-term synaptic plasticity is critical for the developmental refinement of neural circuits and for some forms of learning and memory. Although structural remodeling of dendritic spines is associated with the stable expression of long-term potentiation (LTP), the relationship between structural and physiological plasticity remains unclear. To define whether these two processes are related or distinct, we simultaneously monitored EPSPs and dendritic spines, using combined patch-clamp recording and two-photon time-lapse imaging in the same CA1 pyramidal neurons in acute hippocampal slices. We found that theta burst stimulation paired with postsynaptic spiking, which reliably induced LTP, also induced a rapid and persistent expansion of dendritic spines. Like LTP, this expansion was NMDA receptor dependent. Spine expansion occurred even when LTP was inhibited by postsynaptic inhibition of exocytosis or PKA (protein kinase A); however, under these conditions, the spine expansion was unstable and collapsed spontaneously. Furthermore, similar changes in LTP and spine expansion were observed when hippocampal neurons were treated with protein synthesis inhibitors. Like LTP, spine expansion was reversed by low-frequency stimulation (LFS) via a phosphatase-dependent mechanism, but only if the LFS was applied in a critical time window after induction. These results indicate that the initial expression of LTP and spine expansion is dissociable, but there is a high degree of mechanistic overlap between the stabilization of structural plasticity and LTP.

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Section: Spine Expansion Occurs But Does Not Persist Under Conditionssupporting

confidence: 87%

Section: Spine Stabilization and Ltp Consolidation Are Both Disruptedmentioning

confidence: 99%

Section: Spine Stabilization and Ltp Consolidation Are Both Disruptedmentioning

confidence: 99%

See 1 more Smart Citation

Spine Expansion and Stabilization Associated with Long-Term Potentiation

Yang¹,

Wang²,

Frerking³

et al. 2008

J. Neurosci.

188

248

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“…Therefore, the discovery that zaprinast serves as a relatively potent GPR35 agonist (Taniguchi et al, 2006) affects the interpretation of data in which zaprinast was assumed to solely affect cGMP degradation. For example, zaprinast induced a significant depression of basal synaptic transmission in rat hippocampus attributed to elevation of the intracellular cGMP level (Monfort et al, 2002;Makhinson et al, 2006). However, our data provide evidence for the potential modulation of presynaptic Ca 2ϩ channels by zaprinast acting as a GPR35 agonist.…”

Section: Discussionmentioning

confidence: 55%

Inhibition of N-Type Calcium Channels by Activation of GPR35, an Orphan Receptor, Heterologously Expressed in Rat Sympathetic Neurons

Guo

Williams²,

Puhl³

et al. 2007

J Pharmacol Exp Ther

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GPR35 is a G protein-coupled receptor recently "de-orphanized " using high-throughput intracellular calcium measurements in clonal cell lines expressing a chimeric G-protein ␣-subunit. From these screens, kynurenic acid, an endogenous metabolite of tryptophan, and zaprinast, a synthetic inhibitor of cyclic guanosine monophosphate-specific phosphodiesterase, emerged as potential agonists for GPR35. To investigate the coupling of GPR35 to natively expressed neuronal signaling pathways and effectors, we heterologously expressed GPR35 in rat sympathetic neurons and examined the modulation of N-type (Ca V 2.2) calcium channels. In neurons expressing GPR35, calcium channels were inhibited in the absence of overt agonists, indicating a tonic receptor activity. Application of kynurenic acid or zaprinast resulted in robust voltage-dependent calcium current inhibition characteristic of G␤␥-mediated modulation. Both agonist-independent and -dependent effects of GPR35 were blocked by Bordetella pertussis toxin pretreatment indicating the involvement of G i/o proteins. In neurons expressing GPR35a, a short splice variant of GPR35, zaprinast was more potent (EC 50 ϭ 1 M) than kynurenic acid (58 M) but had a similar efficacy (approximately 60% maximal calcium current inhibition). Expression of GPR35b, which has an additional 31 residues at the N terminus, produced similar results but with much greater variability. Both GPR35a and GPR35b appeared to have similar expression patterns when fused to fluorescent proteins. These results suggest a potential role for GPR35 in regulating neuronal excitability and synaptic release.G protein-coupled receptors (GPCRs) comprise one of the largest families of cell surface proteins and represent a major target for both current therapeutic agents and drugs under development. Many cDNA clones are predicted to code for GPCRs based on high sequence similarity, especially in the transmembrane domains, to established GPCRs. For such orphan GPCRs, the identification of agonists, antagonists, and signal transduction pathways represents a major effort by industry for the discovery of novel drug targets (Stadel et al., 1997). GPR35, an orphan GPCR first discovered during a human genomic DNA screen, shares limited sequence homology with purinergic P2Y receptors, nicotinic acid receptor HM74, lysophosphatidic acid receptor GPR23, and an orphan receptor, GPR55. The highest levels of GPR35 mRNA were found in immune and gastrointestinal tissues with only limited expression in lung and neuronal tissues (O'Dowd et al., 1998;Wang et al., 2006). Subsequent to the initial description of GPR35 (now denoted GPR35a), Okumura et al. (2004) isolated a splice variant (GPR35b) from a human gastric cancer cDNA library that coded for an additional 31 amino acids at the N terminus. GPR35a and GPR35b mRNA levels were up-regulated in gastric cancer tissue, suggesting a role for both splice variants in malignant transformation. However, in the absence of an identified agonist, the functional role GPR35 plays in eithe...

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“…Generation of cGMP by NOsGC appears to be a crucial step in NO signaling in the brain (Boulton et al, 1994;Ahern et al, 2002;Monfort et al, 2004;Makhinson et al, 2006). In subcortical areas, several studies demonstrated that the NO-NOsGC-cGMP pathway can either facilitate (Klyachko et al, 2001;Kraus and Prast, 2002;Li et al, 2004) or inhibit (Ozaki et al, 2000) GABAergic neurotransmission.…”

Section: Both Perisomatic and Dendrite Targeting Gabaergic Neurons Comentioning

confidence: 99%

Hippocampal GABAergic Synapses Possess the Molecular Machinery for Retrograde Nitric Oxide Signaling

Szabadits¹,

Cserép²,

Ludányi³

et al. 2007

J. Neurosci.

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Nitric oxide (NO) plays an important role in synaptic plasticity as a retrograde messenger at glutamatergic synapses. Here we describe that, in hippocampal pyramidal cells, neuronal nitric oxide synthase (nNOS) is also associated with the postsynaptic active zones of GABAergic symmetrical synapses terminating on their somata, dendrites, and axon initial segments in both mice and rats. The NO receptor nitric oxide-sensitive guanylyl cyclase (NOsGC) is present in the brain in two functional subunit compositions: ␣ 1 ␤ 1 and ␣ 2 ␤ 1 . The ␤ 1 subunit is expressed in both pyramidal cells and interneurons in the hippocampus. Using immunohistochemistry and in situ hybridization methods, we describe that the ␣ 1 subunit is detectable only in interneurons, which are always positive for ␤ 1 subunit as well; however, pyramidal cells are labeled only for ␤ 1 and ␣ 2 subunits. With double-immunofluorescent staining, we also found that most cholecystokinin-and parvalbumin-positive and smaller proportion of the somatostatin-and nNOS-positive interneurons are ␣ 1 subunit positive. We also found that the ␣ 1 subunit is present in parvalbumin-and cholecystokinin-positive interneuron terminals that establish synapses on somata, dendrites, or axon initial segments. Our results demonstrate that NOsGC, composed of ␣ 1 ␤ 1 subunits, is selectively expressed in different types of interneurons and is present in their presynaptic GABAergic terminals, in which it may serve as a receptor for NO produced postsynaptically by nNOS in the very same synapse.

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A novel role for cyclic guanosine 3′,5′monophosphate signaling in synaptic plasticity: A selective suppressor of protein kinase A-dependent forms of long-term potentiation

Cited by 16 publications

References 59 publications

Spine Expansion and Stabilization Associated with Long-Term Potentiation

Spine Expansion and Stabilization Associated with Long-Term Potentiation

Inhibition of N-Type Calcium Channels by Activation of GPR35, an Orphan Receptor, Heterologously Expressed in Rat Sympathetic Neurons

Hippocampal GABAergic Synapses Possess the Molecular Machinery for Retrograde Nitric Oxide Signaling

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