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- EMDB-23280: Cryo-EM structure of the human adenosine A1 receptor-Gi2-protein ... -

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Entry
Database: EMDB / ID: EMD-23280
TitleCryo-EM structure of the human adenosine A1 receptor-Gi2-protein complex bound to its endogenous agonist and an allosteric ligand
Map dataFinal masked map
Sample
  • Complex: Human adenosine A1 receptor-Gi2-protein complex bound to its endogenous agonist adenosine
    • Protein or peptide: Guanine nucleotide-binding protein G(i) subunit alpha-2
    • Protein or peptide: Chimera protein of Muscarinic acetylcholine receptor M4 and Adenosine receptor A1
    • Protein or peptide: Guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-1
    • Protein or peptide: Guanine nucleotide-binding protein G(I)/G(S)/G(O) subunit gamma-2
  • Ligand: ADENOSINE
  • Ligand: {2-amino-4-[3,5-bis(trifluoromethyl)phenyl]thiophen-3-yl}(4-chlorophenyl)methanone
  • Ligand: water
Keywordssignaling protein / membrane protein / active-state G protein-coupled receptor / adenosine A1 receptor / PAM / allosteric modulator
Function / homology
Function and homology information


positive regulation of nucleoside transport / negative regulation of neurotrophin production / negative regulation of circadian sleep/wake cycle, non-REM sleep / regulation of glomerular filtration / purine nucleoside binding / positive regulation of peptide secretion / negative regulation of mucus secretion / negative regulation of glutamate secretion / negative regulation of long-term synaptic depression / Muscarinic acetylcholine receptors ...positive regulation of nucleoside transport / negative regulation of neurotrophin production / negative regulation of circadian sleep/wake cycle, non-REM sleep / regulation of glomerular filtration / purine nucleoside binding / positive regulation of peptide secretion / negative regulation of mucus secretion / negative regulation of glutamate secretion / negative regulation of long-term synaptic depression / Muscarinic acetylcholine receptors / G protein-coupled acetylcholine receptor activity / positive regulation of lipid catabolic process / negative regulation of synaptic transmission, GABAergic / negative regulation of adenylate cyclase-activating adrenergic receptor signaling pathway / negative regulation of hormone secretion / negative regulation of leukocyte migration / mucus secretion / heterotrimeric G-protein binding / positive regulation of dephosphorylation / regulation of respiratory gaseous exchange by nervous system process / Adenosine P1 receptors / G protein-coupled adenosine receptor activity / regulation of sensory perception of pain / regulation of presynaptic cytosolic calcium ion concentration / negative regulation of calcium ion-dependent exocytosis / adenylate cyclase-inhibiting G protein-coupled acetylcholine receptor signaling pathway / response to purine-containing compound / G protein-coupled adenosine receptor signaling pathway / negative regulation of adenylate cyclase activity / positive regulation of urine volume / positive regulation of potassium ion transport / positive regulation of neural precursor cell proliferation / negative regulation of synaptic transmission / negative regulation of synaptic transmission, glutamatergic / negative regulation of systemic arterial blood pressure / regulation of cardiac muscle cell contraction / triglyceride homeostasis / protein targeting to membrane / long-term synaptic depression / gamma-aminobutyric acid signaling pathway / leukocyte migration / regulation of locomotion / temperature homeostasis / neuronal dense core vesicle / positive regulation of systemic arterial blood pressure / negative regulation of acute inflammatory response / detection of temperature stimulus involved in sensory perception of pain / presynaptic active zone / negative regulation of apoptotic signaling pathway / regulation of calcium ion transport / negative regulation of long-term synaptic potentiation / asymmetric synapse / G protein-coupled receptor signaling pathway, coupled to cyclic nucleotide second messenger / axolemma / phagocytosis / fatty acid homeostasis / negative regulation of lipid catabolic process / Adenylate cyclase inhibitory pathway / lipid catabolic process / positive regulation of vascular associated smooth muscle cell proliferation / heat shock protein binding / response to nutrient / calyx of Held / hippocampal mossy fiber to CA3 synapse / positive regulation of superoxide anion generation / excitatory postsynaptic potential / Regulation of insulin secretion / apoptotic signaling pathway / G protein-coupled receptor binding / adenylate cyclase-inhibiting G protein-coupled receptor signaling pathway / terminal bouton / G-protein beta/gamma-subunit complex binding / Olfactory Signaling Pathway / cognition / Activation of the phototransduction cascade / G beta:gamma signalling through PLC beta / Presynaptic function of Kainate receptors / Thromboxane signalling through TP receptor / G protein-coupled acetylcholine receptor signaling pathway / adenylate cyclase-activating G protein-coupled receptor signaling pathway / G-protein activation / Activation of G protein gated Potassium channels / Inhibition of voltage gated Ca2+ channels via Gbeta/gamma subunits / Prostacyclin signalling through prostacyclin receptor / G beta:gamma signalling through CDC42 / Glucagon signaling in metabolic regulation / G beta:gamma signalling through BTK / Synthesis, secretion, and inactivation of Glucagon-like Peptide-1 (GLP-1) / ADP signalling through P2Y purinoceptor 12 / Sensory perception of sweet, bitter, and umami (glutamate) taste / photoreceptor disc membrane / Glucagon-type ligand receptors / Adrenaline,noradrenaline inhibits insulin secretion / Vasopressin regulates renal water homeostasis via Aquaporins / G alpha (z) signalling events / Glucagon-like Peptide-1 (GLP1) regulates insulin secretion / cellular response to catecholamine stimulus / vasodilation / ADORA2B mediated anti-inflammatory cytokines production / ADP signalling through P2Y purinoceptor 1
Similarity search - Function
Adenosine A1 receptor / Muscarinic acetylcholine receptor M4 / Muscarinic acetylcholine receptor family / Adenosine receptor / G-protein alpha subunit, group I / Serpentine type 7TM GPCR chemoreceptor Srsx / Guanine nucleotide binding protein (G-protein), alpha subunit / G protein alpha subunit, helical insertion / G-protein alpha subunit / G-alpha domain profile. ...Adenosine A1 receptor / Muscarinic acetylcholine receptor M4 / Muscarinic acetylcholine receptor family / Adenosine receptor / G-protein alpha subunit, group I / Serpentine type 7TM GPCR chemoreceptor Srsx / Guanine nucleotide binding protein (G-protein), alpha subunit / G protein alpha subunit, helical insertion / G-protein alpha subunit / G-alpha domain profile. / G protein alpha subunit / G-protein, gamma subunit / G-protein gamma subunit domain profile. / G-protein gamma-like domain / G-protein gamma-like domain superfamily / GGL domain / G protein gamma subunit-like motifs / GGL domain / Guanine nucleotide-binding protein, beta subunit / G-protein, beta subunit / G-protein coupled receptors family 1 signature. / G protein-coupled receptor, rhodopsin-like / GPCR, rhodopsin-like, 7TM / G-protein coupled receptors family 1 profile. / 7 transmembrane receptor (rhodopsin family) / G-protein beta WD-40 repeat / WD40 repeat, conserved site / Trp-Asp (WD) repeats signature. / WD domain, G-beta repeat / Trp-Asp (WD) repeats profile. / Trp-Asp (WD) repeats circular profile. / WD40 repeats / WD40 repeat / WD40-repeat-containing domain superfamily / WD40/YVTN repeat-like-containing domain superfamily / P-loop containing nucleoside triphosphate hydrolase
Similarity search - Domain/homology
Guanine nucleotide-binding protein G(i) subunit alpha-2 / Muscarinic acetylcholine receptor M4 / Adenosine receptor A1 / Guanine nucleotide-binding protein G(I)/G(S)/G(O) subunit gamma-2 / Guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-1
Similarity search - Component
Biological speciesHomo sapiens (human)
Methodsingle particle reconstruction / cryo EM / Resolution: 3.2 Å
AuthorsDraper-Joyce CJ / Danev R
Funding support Australia, 2 items
OrganizationGrant numberCountry
National Health and Medical Research Council (NHMRC, Australia) Australia
Australian Research Council (ARC) Australia
CitationJournal: Nature / Year: 2021
Title: Positive allosteric mechanisms of adenosine A receptor-mediated analgesia.
Authors: Christopher J Draper-Joyce / Rebecca Bhola / Jinan Wang / Apurba Bhattarai / Anh T N Nguyen / India Cowie-Kent / Kelly O'Sullivan / Ling Yeong Chia / Hariprasad Venugopal / Celine Valant / ...Authors: Christopher J Draper-Joyce / Rebecca Bhola / Jinan Wang / Apurba Bhattarai / Anh T N Nguyen / India Cowie-Kent / Kelly O'Sullivan / Ling Yeong Chia / Hariprasad Venugopal / Celine Valant / David M Thal / Denise Wootten / Nicolas Panel / Jens Carlsson / Macdonald J Christie / Paul J White / Peter Scammells / Lauren T May / Patrick M Sexton / Radostin Danev / Yinglong Miao / Alisa Glukhova / Wendy L Imlach / Arthur Christopoulos /
Abstract: The adenosine A receptor (AR) is a promising therapeutic target for non-opioid analgesic agents to treat neuropathic pain. However, development of analgesic orthosteric AR agonists has failed because ...The adenosine A receptor (AR) is a promising therapeutic target for non-opioid analgesic agents to treat neuropathic pain. However, development of analgesic orthosteric AR agonists has failed because of a lack of sufficient on-target selectivity as well as off-tissue adverse effects. Here we show that [2-amino-4-(3,5-bis(trifluoromethyl)phenyl)thiophen-3-yl)(4-chlorophenyl)methanone] (MIPS521), a positive allosteric modulator of the AR, exhibits analgesic efficacy in rats in vivo through modulation of the increased levels of endogenous adenosine that occur in the spinal cord of rats with neuropathic pain. We also report the structure of the AR co-bound to adenosine, MIPS521 and a G heterotrimer, revealing an extrahelical lipid-detergent-facing allosteric binding pocket that involves transmembrane helixes 1, 6 and 7. Molecular dynamics simulations and ligand kinetic binding experiments support a mechanism whereby MIPS521 stabilizes the adenosine-receptor-G protein complex. This study provides proof of concept for structure-based allosteric drug design of non-opioid analgesic agents that are specific to disease contexts.
History
DepositionJan 12, 2021-
Header (metadata) releaseSep 8, 2021-
Map releaseSep 8, 2021-
UpdateNov 13, 2024-
Current statusNov 13, 2024Processing site: RCSB / Status: Released

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Structure visualization

Movie
  • Surface view with section colored by density value
  • Surface level: 0.02
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  • Surface level: 0.02
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  • Surface view with fitted model
  • Atomic models: PDB-7ld3
  • Surface level: 0.02
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Structure viewerEM map:
SurfViewMolmilJmol/JSmol
Supplemental images

emd_23280.png

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Map

FileDownload / File: emd_23280.map.gz / Format: CCP4 / Size: 64 MB / Type: IMAGE STORED AS FLOATING POINT NUMBER (4 BYTES)
AnnotationFinal masked map
Projections & slices

Image control

Size
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AxesZ (Sec.)Y (Row.)X (Col.)
0.83 Å/pix.
x 256 pix.
= 211.456 Å		0.83 Å/pix.
x 256 pix.
= 211.456 Å		0.83 Å/pix.
x 256 pix.
= 211.456 Å

Surface

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Images are generated by Spider.

Voxel sizeX=Y=Z: 0.826 Å
Density

Histogram

Histogram (log scale)
Contour LevelBy AUTHOR: 0.02 / Movie #1: 0.02
Minimum - Maximum-0.10217636 - 0.15523219
Average (Standard dev.)0.0002214758 (±0.003651534)
SymmetrySpace group: 1
Details

EMDB XML:

Map geometry
Axis orderXYZ
Origin000
Dimensions256256256
Spacing256256256
CellA=B=C: 211.456 Å
α=β=γ: 90.0 °

CCP4 map header:

modeImage stored as Reals
Å/pix. X/Y/Z0.8260.8260.826
M x/y/z256256256
origin x/y/z0.0000.0000.000
length x/y/z211.456211.456211.456
α/β/γ90.00090.00090.000
start NX/NY/NZ000
NX/NY/NZ300300300
MAP C/R/S123
start NC/NR/NS000
NC/NR/NS256256256
D min/max/mean-0.1020.1550.000

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Supplemental data

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Mask #1

Fileemd_23280_msk_1.map
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Additional map: Final Refine3D map

Fileemd_23280_additional_1.map
AnnotationFinal Refine3D map
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Half map: Final Refine3D halfmap 1

Fileemd_23280_half_map_1.map
AnnotationFinal Refine3D halfmap 1
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AxesZYX

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Histogram

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Half map: Final Refine3D halfmap 1

Fileemd_23280_half_map_2.map
AnnotationFinal Refine3D halfmap 1
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Sample components

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Entire : Human adenosine A1 receptor-Gi2-protein complex bound to its endo...

EntireName: Human adenosine A1 receptor-Gi2-protein complex bound to its endogenous agonist adenosine
Components
  • Complex: Human adenosine A1 receptor-Gi2-protein complex bound to its endogenous agonist adenosine
    • Protein or peptide: Guanine nucleotide-binding protein G(i) subunit alpha-2
    • Protein or peptide: Chimera protein of Muscarinic acetylcholine receptor M4 and Adenosine receptor A1
    • Protein or peptide: Guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-1
    • Protein or peptide: Guanine nucleotide-binding protein G(I)/G(S)/G(O) subunit gamma-2
  • Ligand: ADENOSINE
  • Ligand: {2-amino-4-[3,5-bis(trifluoromethyl)phenyl]thiophen-3-yl}(4-chlorophenyl)methanone
  • Ligand: water

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Supramolecule #1: Human adenosine A1 receptor-Gi2-protein complex bound to its endo...

SupramoleculeName: Human adenosine A1 receptor-Gi2-protein complex bound to its endogenous agonist adenosine
type: complex / ID: 1 / Parent: 0 / Macromolecule list: #1-#4
Source (natural)Organism: Homo sapiens (human)

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Macromolecule #1: Guanine nucleotide-binding protein G(i) subunit alpha-2

MacromoleculeName: Guanine nucleotide-binding protein G(i) subunit alpha-2
type: protein_or_peptide / ID: 1 / Number of copies: 1 / Enantiomer: LEVO
Source (natural)Organism: Homo sapiens (human)
Molecular weightTheoretical: 40.502863 KDa
Recombinant expressionOrganism: Trichoplusia ni (cabbage looper)
SequenceString: MGCTVSAEDK AAAERSKMID KNLREDGEKA AREVKLLLLG AGESGKNTIV KQMKIIHEDG YSEEECRQYR AVVYSNTIQS IMAIVKAMG NLQIDFADPS RADDARQLFA LSCTAEEQGV LPDDLSGVIR RLWADHGVQA CFGRSREYQL NDSAAYYLND L ERIAQSDY ...String:
MGCTVSAEDK AAAERSKMID KNLREDGEKA AREVKLLLLG AGESGKNTIV KQMKIIHEDG YSEEECRQYR AVVYSNTIQS IMAIVKAMG NLQIDFADPS RADDARQLFA LSCTAEEQGV LPDDLSGVIR RLWADHGVQA CFGRSREYQL NDSAAYYLND L ERIAQSDY IPTQQDVLRT RVKTTGIVET HFTFKDLHFK MFDVGAQRSE RKKWIHCFEG VTAIIFCVAL SAYDLVLAED EE MNRMHAS MKLFDSICNN KWFTDTSIIL FLNKKDLFEE KITHSPLTIC FPEYTGANKY DEAASYIQSK FEDLNKRKDT KEI YTHFTC STDTKNVQFV FDAVTDVIIK NNLKDCGLF

UniProtKB: Guanine nucleotide-binding protein G(i) subunit alpha-2

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Macromolecule #2: Chimera protein of Muscarinic acetylcholine receptor M4 and Adeno...

MacromoleculeName: Chimera protein of Muscarinic acetylcholine receptor M4 and Adenosine receptor A1
type: protein_or_peptide / ID: 2 / Number of copies: 1 / Enantiomer: LEVO
Source (natural)Organism: Homo sapiens (human)
Molecular weightTheoretical: 43.26102 KDa
Recombinant expressionOrganism: Trichoplusia ni (cabbage looper)
SequenceString: MKTIIALSYI FCLVFADYKD DDDAMGANFT PVNGSSGNQS VRLVTSSSLE VLFQGPPPSI SAFQAAYIGI EVLIALVSVP GNVLVIWAV KVNQALRDAT FCFIVSLAVA DVAVGALVIP LAILINIGPQ TYFHTCLMVA CPVLILTQSS ILALLAIAVD R YLRVKIPL ...String:
MKTIIALSYI FCLVFADYKD DDDAMGANFT PVNGSSGNQS VRLVTSSSLE VLFQGPPPSI SAFQAAYIGI EVLIALVSVP GNVLVIWAV KVNQALRDAT FCFIVSLAVA DVAVGALVIP LAILINIGPQ TYFHTCLMVA CPVLILTQSS ILALLAIAVD R YLRVKIPL RYKMVVTPRR AAVAIAGCWI LSFVVGLTPM FGWNNLSAVE RAWAANGSMG EPVIKCEFEK VISMEYMVYF NF FVWVLPP LLLMVLIYLE VFYLIRKQLN KKVSASSGDP QKYYGKELKI AKSLALILFL FALSWLPLHI LNCITLFCPS CHK PSILTY IAIFLTHGNS AMNPIVYAFR IQKFRVTFLK IWNDHFRCQP APPIDEDLPE ERPDDHHHHH H

UniProtKB: Muscarinic acetylcholine receptor M4, Adenosine receptor A1

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Macromolecule #3: Guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-1

MacromoleculeName: Guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-1
type: protein_or_peptide / ID: 3 / Number of copies: 1 / Enantiomer: LEVO
Source (natural)Organism: Homo sapiens (human)
Molecular weightTheoretical: 38.534062 KDa
Recombinant expressionOrganism: Trichoplusia ni (cabbage looper)
SequenceString: MHHHHHHGSS GSELDQLRQE AEQLKNQIRD ARKACADATL SQITNNIDPV GRIQMRTRRT LRGHLAKIYA MHWGTDSRLL VSASQDGKL IIWDSYTTNK VHAIPLRSSW VMTCAYAPSG NYVACGGLDN ICSIYNLKTR EGNVRVSREL AGHTGYLSCC R FLDDNQIV ...String:
MHHHHHHGSS GSELDQLRQE AEQLKNQIRD ARKACADATL SQITNNIDPV GRIQMRTRRT LRGHLAKIYA MHWGTDSRLL VSASQDGKL IIWDSYTTNK VHAIPLRSSW VMTCAYAPSG NYVACGGLDN ICSIYNLKTR EGNVRVSREL AGHTGYLSCC R FLDDNQIV TSSGDTTCAL WDIETGQQTT TFTGHTGDVM SLSLAPDTRL FVSGACDASA KLWDVREGMC RQTFTGHESD IN AICFFPN GNAFATGSDD ATCRLFDLRA DQELMTYSHD NIICGITSVS FSKSGRLLLA GYDDFNCNVW DALKADRAGV LAG HDNRVS CLGVTDDGMA VATGSWDSFL KIWN

UniProtKB: Guanine nucleotide-binding protein G(I)/G(S)/G(T) subunit beta-1

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Macromolecule #4: Guanine nucleotide-binding protein G(I)/G(S)/G(O) subunit gamma-2

MacromoleculeName: Guanine nucleotide-binding protein G(I)/G(S)/G(O) subunit gamma-2
type: protein_or_peptide / ID: 4 / Number of copies: 1 / Enantiomer: LEVO
Source (natural)Organism: Homo sapiens (human)
Molecular weightTheoretical: 7.861143 KDa
Recombinant expressionOrganism: Trichoplusia ni (cabbage looper)
SequenceString:
MASNNTASIA QARKLVEQLK MEANIDRIKV SKAAADLMAY CEAHAKEDPL LTPVPASENP FREKKFFCAI L

UniProtKB: Guanine nucleotide-binding protein G(I)/G(S)/G(O) subunit gamma-2

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Macromolecule #5: ADENOSINE

MacromoleculeName: ADENOSINE / type: ligand / ID: 5 / Number of copies: 1 / Formula: ADN
Molecular weightTheoretical: 267.241 Da
Chemical component information

ChemComp-ADN:
ADENOSINE

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Macromolecule #6: {2-amino-4-[3,5-bis(trifluoromethyl)phenyl]thiophen-3-yl}(4-chlor...

MacromoleculeName: {2-amino-4-[3,5-bis(trifluoromethyl)phenyl]thiophen-3-yl}(4-chlorophenyl)methanone
type: ligand / ID: 6 / Number of copies: 1 / Formula: XTD
Molecular weightTheoretical: 449.797 Da
Chemical component information

ChemComp-XTD:
{2-amino-4-[3,5-bis(trifluoromethyl)phenyl]thiophen-3-yl}(4-chlorophenyl)methanone

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Macromolecule #7: water

MacromoleculeName: water / type: ligand / ID: 7 / Number of copies: 1 / Formula: HOH
Molecular weightTheoretical: 18.015 Da
Chemical component information

ChemComp-HOH:
WATER

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Experimental details

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Structure determination

Methodcryo EM
Processingsingle particle reconstruction
Aggregation stateparticle

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Sample preparation

BufferpH: 7.5
VitrificationCryogen name: ETHANE-PROPANE / Chamber humidity: 100 % / Chamber temperature: 277 K / Instrument: FEI VITROBOT MARK IV

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Electron microscopy

MicroscopeFEI TITAN KRIOS
Image recordingFilm or detector model: GATAN K3 (6k x 4k) / Detector mode: COUNTING / Digitization - Dimensions - Width: 3838 pixel / Digitization - Dimensions - Height: 3710 pixel / Average exposure time: 8.0 sec. / Average electron dose: 50.0 e/Å2
Electron beamAcceleration voltage: 300 kV / Electron source: FIELD EMISSION GUN
Electron opticsIllumination mode: OTHER / Imaging mode: BRIGHT FIELD
Sample stageSpecimen holder model: FEI TITAN KRIOS AUTOGRID HOLDER / Cooling holder cryogen: NITROGEN
Experimental equipment
Model: Titan Krios / Image courtesy: FEI Company

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Image processing

Startup modelType of model: PDB ENTRY
PDB model - PDB ID:

6d9h

Final reconstructionResolution.type: BY AUTHOR / Resolution: 3.2 Å / Resolution method: FSC 0.143 CUT-OFF / Number images used: 683928
Initial angle assignmentType: MAXIMUM LIKELIHOOD
Final angle assignmentType: PROJECTION MATCHING
FSC plot (resolution estimation)

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