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Von Zastrow, M.

Publications and source records attributed to Von Zastrow, M..

14 recordsLinked to original sources

Distinct activation mechanisms underlie ligand efficacy at a GPCR

Ligands that bind to the same G protein-coupled receptor (GPCR) can produce widely different levels of signaling. These differences in efficacy are central to pharmacology, yet how a receptor sequence determines signaling level remains incompletely understood. Here we develop a deep mutational pharmacology approach to measure how each residue in the -opioid receptor (OR) shapes responses to 15 opioids, yielding ~400,000 measurements of variant effects on signaling and expression, including full concentration-response series for three agonists. Mutational effects on potency are strongest near the orthosteric pocket, whereas effects on efficacy extend through the transmembrane core and intracellular face. Ligands share many functional determinants, but sensitivity to mutation differs with efficacy. As efficacy decreases, the residues required for signaling shift from the binding pocket towards the intracellular face; partial agonists therefore depend on residues that are dispensable for full agonists. Mutations can broadly increase receptor responses, allowing antagonists such as naloxone to produce signaling comparable to a full agonist and increasing the efficacy of partial agonist ligands. Combined mutations can also reorder the relative efficacies of ligands, showing that sequence changes reshape pharmacological differences rather than simply increasing or decreasing all responses together. These findings support a model in which ligands of different efficacy activate the receptor through distinct allosteric mechanisms which are determined by residues distributed across the receptor. Mapping these contributions across diverse ligands with deep mutational pharmacology provides a way to understand how one receptor converts molecular recognition into a range of signaling outputs.

biophysics↗

Primary cilia facilitate GPCR neurotransmission through the canonical cAMP cascade

The primary cilium is increasingly recognized to be a discrete site for initiating neurotransmission through G protein-coupled receptors (GPCRs), yet how such neurotransmission is propagated downstream remains unclear. A canonical pathway of downstream GPCR neurotransmission is the cyclic AMP (cAMP) / cAMP-dependent protein kinase (PKA) cascade. While cAMP can be locally generated in cilia and produce important effects that are functionally compartmentalized there, neurotransmission through GPCRs must propagate to effectors outside of cilia. Thus, a prevailing current view is that ciliary neurotransmission is restricted to non-canonical, cAMP-dependent pathways. Revisiting this view, we show here that the primary cilium of striatal medium spiny neurons is a major site from which endogenous D1 dopamine receptors initiate cAMP and PKA activity elevations that propagate throughout the extraciliary cytoplasm. We also show that the primary cilium spatially aligns essentially this entire long-range signaling axis from intercalating with numerous dopaminergic axon varicosities that initiate neurotransmission to enforcing proximity with somatic PKA stores that are activated by cAMP downstream. Together, these results extend the concept of ciliary neurotransmission to dopaminergic signaling in striatal neurons and reveal that, in this system, the primary cilium facilitates rather than restricts neurotransmission through the canonical cAMP / PKA cascade.

neuroscience↗

Temporal coding expands the bandwidth of GPCR-mediated neuromodulation

The advent of modern transcriptomic approaches has revealed a breadth of neuromodulatory G protein-coupled receptor (GPCR) co-expression far exceeding what was previously thought. This raises a fundamental question about neuromodulatory system architecture because there is a much smaller number of available G protein transducers. Does this impose an information bottleneck, or can a single transducer pathway distinguish the effects of different neuromodulators? We addressed this question by focusing on four GPCRs that are natively co-expressed in essentially all hippocampal pyramidal neurons and that signal through the canonical Gs-coupled cyclic AMP (cAMP) cascade. We show that each GPCR produces a similar cAMP elevation upon acute activation but the effects observed at downstream steps diverge, to the point that the GPCRs differ dramatically in their ability to drive a transcriptional response. We also show that they differ in their ability to maintain functional responsiveness, with neuropeptide receptors remaining responsive for hours but monoamine receptors rapidly losing responsiveness. We conclude that the effective chemical bandwidth of cellular neuromodulation by GPCRs is not limited by the number of available transducers, and that there exists additional temporal coding which enables individual neurons to distinguish a richer neuromodulatory input.

neuroscience↗

An engineered nanobody inhibitor for molecular-to-circuit control of opioid receptor function

Opioid receptors (ORs) orchestrate pain relief, reward, and dependence, yet their signaling arises from diverse cell types and subcellular compartments that cannot be selectively interrogated with existing pharmacological or genetic approaches. Single-domain antibodies, or nanobodies (Nbs), can probe receptor states, but their potential as tools for controlling native receptor signaling at the system level has remained unexplored. Here, we engineer a suite of high-affinity intracellular Nbs that bind active ORs through structure-guided evolution and in silico design. Iterative optimization yields Nb64, a potent inhibitor that rapidly suppresses transducer engagement, receptor internalization, and downstream signaling, including endogenous pathways in neuronal cells. Organelle targeting highlights Nb64s capacity to control OR activity with subcellular precision, while bio-reversible cell-penetrating peptide (CPP) conjugation enables non-genetic cytosolic delivery. Cell-type-specific expression of Nb64 in VTA interneurons attenuates fentanyl-evoked dopamine release and behavioral responses in mice, demonstrating targeted control of opioid actions in vivo. Nb64 provides a versatile strategy for dissecting OR biology and establishes a generalizable framework for precision inhibition of native GPCR signaling in vivo.

neuroscience↗

Endocytosis sculpts distinct cAMP signal transduction by endogenously coexpressed GPCRs

Many G protein-coupled receptors (GPCRs) initiate a second phase of signaling after activation-induced endocytosis, but GPCRs vary considerably in their ability to internalize when activated. Here we show that this fundamental trafficking difference distinguishes the downstream signaling profiles of natively co-expressed GPCRs through the cAMP cascade. We focus on signaling to the nucleus stimulated by three different Gs-coupled GPCRs that are each endogenously co-expressed in human embryonic kidney cells but differ in their ability to internalize after activation: the adenosine-2B receptor that does not detectably internalize, the vasoactive intestinal peptide receptor-1 that internalizes very rapidly, and the {beta}2-adrenergic receptor that internalizes less rapidly. We show that each GPCR produces a distinct signaling profile differentiated by endocytosis. Our results support a model in which endocytosis compresses chemical information sensed by distinct GPCRs into a spatiotemporal cAMP code by setting receptor-specific differences in the amount and duration of cAMP production from endosomes relative to the plasma membrane and that this is decoded downstream in the pathway through sequential layers of processing by cytoplasmic and nuclear PKA activities. We propose that this biological information processing strategy has parallels to how computational encoder-decoder (autoencoder) networks denoise and recognize latent patterns in complex electrical signals.

cell biology↗

Opioid receptors reveal a discrete cellular mechanism of endosomal G protein activation

Many GPCRs initiate a second phase of G protein-mediated signaling from endosomes, which inherently requires an increase in G protein activity on the endosome surface. Gs-coupled GPCRs are thought to achieve this by internalizing and allosterically activating cognate G proteins again on the endosome membrane. Here we demonstrate that the -opioid receptor (MOR), a Gi-coupled GPCR, increases endosomal G protein activity in a different way. Leveraging conformational biosensors, we resolve the subcellular activation dynamics of endogenously expressed MOR and Gi/o-subclass G proteins. We show that MOR activation triggers a transient increase of active-state Gi/o on the plasma membrane that is followed by a prolonged increase on endosomes. Contrary to the Gs-coupled GPCR paradigm, however, we show that the MOR-induced increase of active-state Gi/o on endosomes requires neither internalization of MOR nor activation of MOR in the endosome membrane. We propose a distinct and additional cellular mechanism for GPCR-triggered elevation of G protein activity on endosomes that is mediated by regulated trafficking of the activated G protein rather than its activating GPCR.

pharmacology and toxicology↗

Spatial organization of adenylyl cyclase and its impact on dopamine signaling in neurons

The cAMP cascade is widely recognized to transduce its physiological effects locally through spatially limited cAMP gradients. However, little is known about how the adenylyl cyclase enzymes, which initiate cAMP gradients, are localized. Here we answer this question in physiologically relevant striatal neurons and delineate how AC localization impacts downstream signaling functions. We show that the major striatal AC isoforms are differentially sorted between ciliary and extraciliary domains of the plasma membrane, and that AC9 is uniquely targeted to endosomes. We identify key sorting determinants in the N-terminal cytoplasmic domain responsible for isoform-specific localization. We also show that AC9-containing endosomes accumulate activated dopamine receptors and form an elaborately intertwined network with juxtanuclear PKA stores bound to Golgi membranes. Finally, we show that endosomal localization is critical for AC9 to selectively elevate PKA activity in the nucleus relative to the cytoplasm. These results reveal a precise spatial landscape of the cAMP cascade in neurons and a key role of AC localization in directing downstream signal transduction to the nucleus.

cell biology↗

A genome-wide CRISPR interference screen using an engineered trafficking biosensor reveals a role for RME-8 in opioid receptor regulation

G protein-coupled receptors (GPCRs) are the largest family of membrane-bound signaling molecules. Activity of these receptors is critically regulated by their trafficking through the endo-lysosomal pathway. Identifying the genes involved in GPCR trafficking is challenging due the complexity of sorting operations and low affinity protein-protein interactions. Here we present a chemical biology fluorescence-based technique to interrogate GPCR trafficking. We show that the engineered enzyme APEX2 is a highly sensitive biosensor for GPCR trafficking to the lysosome, and this trafficking can be monitored through APEX-based activation of fluorogenic substrates such as Amplex UltraRed (AUR). We used this approach to perform a genome-wide CRISPR interference screen focused on the delta type opioid receptor (DOR), a GPCR which modulates anxiety, depression, and pain. The screen identified 492 genes including known- and novel-regulators of DOR expression and trafficking. We demonstrate that one of the novel genes, RME-8, localizes to early endosomes and plays a critical role in regulating DOR trafficking to the lysosome. Together, our data demonstrate that GPCR-APEX2/AUR is a flexible and highly sensitive chemical biology platform for genetic interrogation of receptor trafficking.

cell biology↗

A discrete mode of endosomal GPCR signaling that does not require β-arrestin

Many GPCRs are now recognized to initiate a second phase of G protein (Gs) -dependent signaling through the cAMP cascade after endocytosis. A prevailing current view is that endocytosis-promoted signaling from GPCRs is inherently {beta}-arrestin-dependent because {beta}-arrestin is necessary for receptors to internalize and, for some GPCRs, it also promotes Gs activation on endosomes. Here we revise this view by showing that the vasoactive intestinal peptide receptor 1 (VIPR1), a prototypic secretin-family polypeptide hormone receptor, remains bound to {beta}-arrestin after endocytosis but does not require {beta}-arrestin either to internalize or to generate an endosomal signal. {beta}-arrestin instead resolves the endosomal signal into a temporally separated cAMP peak, and it does so by attenuating signaling from the plasma membrane without detectably affecting the endosomal response. The mechanistic basis for this location-specific difference in {beta}-arrestin function is the formation of distinct VIPR1/{beta}-arrestin complexes at each location. The signal-attenuating complex formed at the plasma membrane does not require GRK-mediated phosphorylation of receptors, while the signaling-neutral complex present on the endosome membrane, in contrast, is GRK-dependent. To our knowledge, the present results provide the first direct demonstration that endosomal GPCR signaling can occur in the complete absence of {beta}-arrestin. They also reveal a discrete role of {beta}-arrestin in sculpting the spatiotemporal profile of cellular GPCR - G protein signaling through the location-specific formation or remodeling of GPCR/{beta}-arrestin complexes.

cell biology↗

Endocytic trafficking determines cellular tolerance of presynaptic opioid signaling

Opioid tolerance is well described physiologically but its mechanistic basis remains incompletely understood. An important site of opioid action in vivo is the presynaptic terminal, where opioids inhibit transmitter release. This response characteristically resists desensitization over minutes yet becomes gradually tolerant over hours, and how this is possible remains unknown. Here we delineate a cellular mechanism underlying this longer-term form of opioid tolerance. Our results support a model in which presynaptic tolerance is mediated by a gradual depletion of cognate receptors from the axon surface through iterative rounds of receptor endocytosis and recycling. For the -opioid receptor (MOR), we show that the agonist-induced endocytic process which initiates iterative receptor cycling requires GRK2/3-mediated phosphorylation of the receptors cytoplasmic tail, and that partial or biased agonist drugs which have reduced ability to drive phosphorylation-dependent endocytosis in terminals produce correspondingly less presynaptic tolerance. We then show that the {delta}-opioid receptor (DOR) conforms to the same general paradigm except that endocytosis of DOR from the presynapse, in marked contrast to MOR, does not require phosphorylation of the receptors cytoplasmic tail. Further, we show that DOR recycles less efficiently than MOR in axons and, consistent with this, that DOR tolerance develops more strongly. Together, these results delineate a cellular basis for the development of presynaptic tolerance to opioids and describe a methodology useful for investigating presynaptic neuromodulation more broadly.

neuroscience↗

Profiling the diversity of agonist-selective effects on the proximal proteome environment of G protein-coupled receptors

The mu opioid receptor (OR), a prototypic member of the large G protein-coupled receptor (GPCR) family, represents an important target of therapeutic and abused drugs. To date, most of our understanding of OR activity has focused on signal transducers and regulatory molecules including G proteins, GPCR kinases, and beta-arrestins. Yet it is clear that signaling through the OR is coordinated by additional proteins recruited into the proximal interaction network of the activated receptor, which have largely remained invisible given the lack of technologies to interrogate these networks systematically. Here, we implement a quantitative proteomics pipeline leveraging the chemical diversity of OR agonists and APEX-based proximity labeling to investigate the protein networks that underlie OR signaling. We leverage a novel computational framework to extract subcellular location, trafficking, and functional partners of GPCR activity from the proximity labeling datasets. Applying this unbiased, systematic approach to the OR, we demonstrate that opioid agonists exert differences in the OR proximal proteome mediated by endocytosis and subsequent endosomal sorting, exemplified by VPS35 and COMMD3. Moreover, we identify two novel OR network components, EYA4 and KCTD12, that are recruited into the receptor proximal network irrespective of the activating ligand and independent of receptor trafficking but based on receptor-triggered G protein activation. We provide functional evidence that these network components form a previously unrecognized buffering system for G protein activity which broadly modulates cellular GPCR signaling.

systems biology↗

Membrane phosphoinositides stabilize GPCR-arrestin complexes and offer temporal control of complex assembly and dynamics

Binding of arrestin to phosphorylated G protein-coupled receptors (GPCRs) is crucial for modulating signaling. Once internalized some GPCRs may complex with arrestin, while others interact transiently; this difference affects receptor signaling and recycling. Cell-based and in vitro biophysical assays reveal the role of membrane phosphoinositides (PIPs) in arrestin recruitment and GPCR-arrestin complex dynamics. We find that GPCRs broadly stratify into two groups, one requiring PIP-binding for arrestin recruitment and one that does not. Plasma membrane PIPs potentiate an active conformation of arrestin and stabilize GPCR-arrestin complexes by promoting a receptor core-engaged state of the complex. As allosteric modulators of GPCR-arrestin complex dynamics, membrane PIPs allow for additional conformational diversity beyond that imposed by GPCR phosphorylation alone. The dependance on membrane PIPs provides a mechanism for arrestin release from transiently associated GPCRs, allowing their rapid recycling, while explaining how stably associated GPCRs are able to engage G proteins at endosomes.

biochemistry↗

G protein-regulated endocytic trafficking of adenylyl cyclase type 9

GPCRs are increasingly recognized to initiate signaling via heterotrimeric G proteins as they move through the endocytic network, but little is known about how relevant G protein effectors are localized. Here we report dynamic trafficking of adenylyl cyclase type 9 (AC9) from the plasma membrane to endosomes, while adenylyl cyclase type 1 (AC1) remains in the plasma membrane, and stimulation of AC9 trafficking by ligand-induced activation of Gs-coupled GPCRs or Gs. AC9 transits a similar dynamin-dependent early endocytic pathway as activated GPCRs but, in contrast to GPCR trafficking which is regulated by {beta}-arrestin but not Gs, AC9 trafficking is regulated by Gs but not {beta}-arrestin. We also show that AC9, but not AC1, contributes to cAMP production from endosomes. These results reveal dynamic and isoform-specific trafficking of adenylyl cyclase in the endocytic network, and a discrete role of a heterotrimeric G protein in controlling subcellular location of a relevant effector.

cell biology↗

Time-gated detection of protein-protein interactions with transcriptional readout

Transcriptional assays such as yeast two hybrid, split ubiquitin, and Tango that convert transient protein-protein interactions (PPIs) in cells into stable expression of transgenes are powerful tools for PPI discovery, high-throughput screens, and analysis of large cell populations. However, these assays frequently suffer from high background and they lose all information about PPI dynamics. To address these limitations, we developed a light-gated transcriptional assay for PPI detection called PPI-FLARE (PPI-Fast Light- and Activity-Regulated Expression). PPI-FLARE requires both a PPI to deliver TEV protease proximal to its cleavage peptide, and externally-applied blue light to uncage the cleavage peptide, in order to release a membrane-tethered transcription factor (TF) for translocation to the nucleus. We used PPI-FLARE to detect the ligand-induced association of 12 different PPIs in living mammalian cells, with a temporal resolution of 5 minutes and a {+/-}ligand signal ratio up to 37. By systematically shifting the light irradiation window, we could reconstruct PPI time-courses, distinguishing between GPCRs that engage in transient versus sustained interactions with the cytosolic effector arrestin. When combined with FACS, PPI-FLARE enabled >100-fold enrichment of cells experiencing a specific GPCR-arrestin PPI during a short 10-minute light window over cells missing that PPI during the same time window. Due to its high specificity, sensitivity, and generality, PPI-FLARE should be a broadly useful tool for PPI analysis and discovery.

bioengineering↗