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Research Background

What are GIRK channels?

GIRK (also referred to as Kir3) channels are G protein-gated inwardly rectifying potassium channels. Like all inward rectifiers, the flow of inward current through GIRK channels is much larger than the outward flow – the small outward flow of potassium current reduces neuronal membrane excitability. Four GIRK channel subunits (GIRK1-GIRK4) have been identified in mammals [1]. GIRK1 co-assembles with GIRK2, GIRK3, or GIRK4 to produce functional channels [2-5]. In neurons, three different splice variants of GIRK2 (GIRK2a, GIRK2b and GIRK2c) channels exist [6]; each splice variant can form homotetramers in heterologous expression systems [4] and in neurons [7]. In the brain, GIRK channels comprise the he slow inhibitory postsynaptic potential (sIPSP), a major inhibitory pathway. The sIPSP is important for altering the firing behavior of neurons, and opposes excitatory inputs from glutamatergic synapses [8, 9]. Figure 1. Overview of projects in Slesinger lab. Many inhibitory neurotransmitters work by opening GIRK channels. Our current studies examine all aspects of GIRK channel function, ranging from molecular structure-function experiments, to cellular regulation and physiology of GIRK channel in neurons, to animal models of drug addiction (Figure 1).


GIRK channels generate the GABA-B receptor-dependent slow inhibitory postsynaptic potential (sIPSP; also referred to as slow inhibitory postsynaptic current – sIPSC) in hippocampus [9]. The sIPSP constitutes a major form of inhibitory signaling in the brain. This form of slow inhibition contrasts with the fast inhibition produced by activation of GABA-A or glycine receptors. Spontaneous release of GABA can trigger fast inhibitory post synaptic currents but these synaptic levels of GABA are too low to activate GABA-B receptors and open GIRK channels. Electrophysiological studies have suggested that sustained activation of GABA interneurons leads to pooling and ‘spillover’ of GABA, which then activates GABA-B receptors and GIRK channels located perisynaptically [10, 11]. Cell-attached patch-clamp recordings demonstrate GIRK channels on the dendritic shaft [12]. Recent immuno-electron microscopy (EM) studies indicate that GIRK channels and GABA-B receptors are expressed on the dendritic shaft and also in the dendritic spine [13]. The loss of GIRK-dependent inhibition can therefore significantly alter signaling in the brain. For example, reduced GIRK currents lead to changes in analgesia [14] as well as altering the response to abused drugs [15] and alcohol [16].

In the 1980’s, studies from Hille’s laboratory [17] and from Soejima and Noma laboratories [18] demonstrated that GIRK channels are unique among ion channels – GIRK channels are activated by G proteins through a ‘membrane delimited’ process. At that time, it was not known whether Gα or Gβγ subunits activated the channel, or if the G protein activation was direct (i.e. no intermediary proteins). Although there was agreement on the role of G proteins, a contentious debate grew over whether the Gα or Gβγ subunits mediated the activation [19, 20]. We cloned the first GIRK subunit (Kubo et al., 1993) [21] and published a critical study demonstrating that Gβγ subunits, in fact, and not Gα subunits, directly activate GIRK channels (Reuveny et al., 1994) [22], generating key evidence to resolve the debate. These findings provided one of the first examples of a Gβγ effector and led to the concept that G proteins contain two signaling arms, the Gα and the Gβγ subunits [23]. Two important questions followed from those landmark studies, and have been an area of focus in my lab. First, what is the molecular mechanism underlying Gβγ activation? Second, how do specific G proteins and receptors couple directly to GIRK channels?

What is the molecular mechanism underlying Gβγ activation? Using in vitro protein-protein binding assays and functional electrophysiological analyses of chimeric channels, we identified several regions in the N- and C-terminal domains of GIRK channels involved in Gβγ activation (Finley et al, 2004) [24]. In particular, we discovered a key amino acid in GIRKs that is involved in Gβγ activation but not in Gβγ binding (Finley et al., 2004) [24]. In collaboration with Senyon Choe’s lab, we determined the high-resolution structure of the cytoplasmic domains of GIRK1 and IRK1 channels (Pegan et al, 2005, pleas see press release) [25]. This structure enabled us to directly visualize the putative Gβγ activation domain and also led to important studies on the C-terminal interaction with PDZ domains (Pegan et al., 2007 and see below) [26], mechanisms of inward rectification (Kurata et al., 2007) [27], and mechanism underlying alcohol activation (Pegan et al., 2006) [28]. The molecular mechanism underlying Gβγ activation of GIRK channels, however, has remained a mystery. Recently, we made significant advances in elucidating the mechanism of GIRK channel activation. Our insight came from one of our high-resolution structures of a variant of IRK1 (Pegan et al, 2006) [28]. We observed an alcohol (MPD) bound in a hydrophobic pocket formed at the interface of two adjacent channel subunits. We are currently examining this site for alcohol-dependent activation of GIRK channels.

How do specific G proteins and receptors couple directly to GIRK channels? Stimulation of GPCRs that couple to PTX-sensitive G proteins (e.g. Gαi/o) activates GIRK channels. However, stimulation of GPCRs that couple to PTX-insensitive G proteins (e.g. Gαq, Gαs) does not open GIRK channels. This specificity of receptor coupling has been a conundrum in the G protein field, since activation of any G protein would be expected to liberate Gβγ subunits and activate the channel. We postulated that this type of receptor specificity could be achieved if neurons created a compartment that contained the appropriate GPCRs, G proteins, GIRK channels and other regulatory proteins (a macromolecular signaling complex). Over the last few years, we have completed several studies that provide convincing evidence for a GIRK macromolecular signaling complex (Figure 1). In our first study, we discovered that the Gα subunit directly binds to the GIRK channel (Clancy et al., 2005) [29]. We further showed that the C-terminal domain associated with PTX-sensitive (Gαi/o) but not the PTX-insensitive Gα subunits. We localized the site of Gαi/o binding to a short sequence of amino acids in the C-terminal domain of GIRK channels – this region was distinct from the Gβγ activation site described above. Importantly, mutation of the Gα binding domain attenuated receptor activation of GIRK channels. These data suggested that binding of Gαi/o subunits to the channel is an important step in establishing a specific GIRK/GPCR/PTX-sensitive G protein-signaling pathway. Furthermore, our data suggested that the G protein heterotrimer is docked on the GIRK channel. To test this directly, we measured the possible FRET between CFP/YFP tagged GPCRs, RGS, Gα G-proteins and GIRK channels to assess whether proteins within this complex are physically close. FRET occurs between two fluorophores with overlapping spectral properties when they are situated within 100 Å of each other. To study only the proteins expressed on the plasma membrane, we combined the FRET measurements with total internal reflectance fluorescence (TIRF) microscopy. We found that tagged αBAB receptors and GIRK channels exhibit FRET, supporting the idea of a signaling complex (Fowler et al., 2007) [30]. More recently, we found that RGS2, another Gα binding protein, produces FRET with GIRK3 channels in a complex (Labouebe et al, 2007) [31]. In this study, the formation of a GIRK signaling complex with RGS2 is important for setting the response to abused drugs. Collectively, these studies provide a preponderance of evidence for the existence of a GIRK channel macromolecular signaling complex.

Regulation of GIRK channel macromolecular signaling complex – a new role in drug addiction

We next searched for ways to study a macromolecular signaling complex comprised of natively expressed GPCRs and GIRK channels. Neuronal PC12 cells express M2 muscarinic receptors, GIRK2 channels and PTX-sensitive G proteins (Clancy et al., 2007) [32]. Neuronal PC12 cells stop dividing, adopt a neuronal phenotype, extend neuritis and synthesize and release neurotransmitters following long-term treatment with NGF. In these cells, we demonstrated for the first time that stimulation of muscarinic receptors (i.e. desensitization) leads to internalization of M2 receptors and GIRK channels (Clancy et al., 2007) [32]. Figure 2. Discovery of a drug-sensitive protein, SNX27, that regulates surface expression of GIRK channels.This study provides the first direct evidence for regulation of a natively expressed GIRK/GPCR signaling complex. More recently, we uncovered a novel association between the GABA-B receptor and the M2 muscarinic receptors in this GPCR/signaling complex. By associating directly with M2 receptors, GABA-B receptors can block the M2-dependent desensitization. This association of GABA-B R2 and M2R provides a novel pathway for regulating muscarinic desensitization and represents a previously unrecognized role for GABA-B R2 in neuronal signaling. This model of GPRC/GIRK channel signaling challenges the canonical pathway for stimulation of G proteins, where Gα and Gβγ subunits dissociate from each, following receptor stimulation. The concept of a specific GPRC/GIRK signaling complex is now becoming more widely accepted [33, 34, 35, 36, 37, 38, 39].

We hypothesized that cytoplasmic proteins might regulate the GPCR/GIRK signaling complex. We carried out a search for new GIRK regulating proteins using tandem mass spectrometry (in collaboration with John Yates). We were successful and discovered the first cytoplasmic protein that regulates the surface expression of GIRK channels – sorting nexin 27 (SNX27) (Lunn et al, 2007; Nassirpour et al., 2007 – please see press release) [40, 41]. SNX27 is the only SNX so far that contains a PDZ domain. Interestingly, GIRK channels contain a PDZ binding motif but fail to bind the known ‘classic’ PDZ-containing proteins (e.g. PSD95, SAP97, Chapsyn110). We demonstrated that SNX27 binds directly to GIRK2/3 channels via this PDZ binding motif. Expression of SNX27 in cells reduces the surface expression of GIRK channels. SNX27 is expressed in the brain and colocalizes with endogenous GIRK channels in hippocampal neurons (Lunn et al., 2007) [40]. Thus, regulation of the GIRK channel macromolecular signaling complex may involve a direct interaction with SNX27 (Figure 2).

In addition to SNX27, we have been carrying out studies to identify other proteins that might regulate the expression of GIRK channels in neurons. We discovered that morphine treatment of hippocampal neurons alters the targeting of GIRK channels in hippocampal neurons. GIRK channels are expressed in dendrites of hippocampal pyramidal neurons, where they play an inhibitory role in modulating synaptic activity. Typically, synaptic spines are specialized for only excitatory neurotransmission (i.e. NMDA, AMPA, mGluR, PSD-95) – and contain few GIRK channels. However, we found that stimulation of opioid receptors with morphine (100 μM) for 24 hr or expression of activated CaMKII increases the expression of GIRK2 in the dendritic spines, as revealed by quantitative immunohistochemistry at the light and electron microscopic levels. Functional electrophysiological analyses revealed that agonist-independent basal GIRK currents are larger in morphine- or CaMKII treated neurons. Thus, stimulation of opioid receptors reveals a form of CaMKII-dependent plasticity for the slow inhibitory GIRK pathway in hippocampus. We are currently examining this CaMKII-dependent regulation in more detail and the possible role of SNX27 in mediating the change in GIRK signaling.

Interestingly, SNX27 was identified previously in a search for transcripts upregulated in rodents sensitized to psychostimulants (e.g. cocaine, methamphetamine) [42]. This transcript was referred to as Mrt1, for methamphetamine response transcript. The function of SNX27/Mrt1 was unknown at that time. Our discovery that SNX27 regulates GIRK channels provides new clues into the function of GIRK channels in the brain and a role for GIRK channels in addiction to psychostimulants. Our breakthrough in identifying a regulatory protein for GIRK channels raises many important questions about SNX27 that we will be pursuing in the lab over the next few years.

What is the function of SNX27 in the brain under normal conditions? We plan to study this by up- and down-regulating SNX27 in neurons. What is the mechanism of PDZ binding specificity? We showed that the PDZ domain of SNX27 exhibited binding selectivity for GIRK3 but not for the related IRK1 channels, even though both channels contain a class I PDZ binding motif, ESKV vs. ESEI, respectively (Lunn et al., 2007) [40]. The determinants of this PDZ binding specificity are unknown. What is the role of GIRK channels in psychostimulant addiction? The association between SNX27 and GIRK channels in the VTA leads to the hypothesis that GIRK signaling will be altered in rodents sensitized to psychostimulants.

Link between GIRK channels and addiction

Many drugs of abuse work by altering the signaling of neurotransmitters in the brain, particularly dopamine. For example, methamphetamines enhance the release of dopamine, which stimulates dopamine G protein-coupled receptors that couple, in part, to GIRK channels. The up-regulation of SNX27 with psychostimulants and association with GIRK channels provides one example. Another type of abused drug, gamma-hydroxy butyrate (GHB), is a “club” drug that acts on G-protein-coupled GABA-B receptors, which also couple to GIRK channels in the ventral tegmental area (VTA) and change DA signaling [15]. The VTA is one of the major regions in the brain involved in drug reward and reinforcement. We found that GIRK channels play an important role in mediating the action of GHB. In the VTA, the coupling efficiency for GABA-B receptors to GIRK channels is an order of magnitude weaker in DA neurons (higher EC50) compared to GABA neurons (lower EC50). We also determined that DA neurons express only GIRK2c/GIRK3 and that GIRK2c/3 channels couple less efficiently to GABA-B receptors. GABA neurons, on the other hand, express GIRK1/GIRK2c/GIRK3 subunits. This difference in EC50 can account for whether GABA-B agonists simulate or suppress DA neurons in the VTA. Our findings implicate G-proteins and GIRK channels in drug addiction and serve as the foundation for a future series of experiments (Cruz et al. 2004, please see press release). These studies are part of a long-standing collaboration Dr. Christian Lüscher’s laboratory at Geneva, Switzerland. Recently, we found that the shift in EC50 is also a consequence of the selective expression of RGS2 in DA neurons [31]. Furthermore, we found that RGS2 selectively associates with GIRK3 channels, illustrating the functional importance of a GIRK channel macromolecular signaling complex. These studies raise many important questions about the role for GIRK channels in drug addiction.


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